283

Can body weight supported treadmill training

increase bone mass and reverse muscle atrophy
in individuals with chronic incomplete spinal cord
injury?
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Lora M. Giangregorio, Colin E. Webber, Stuart M. Phillips, Audrey L. Hicks, B.

Catherine Craven, Joanne M. Bugaresti, and Neil McCartney

Abstract: This study evaluates the impact of 12 months of body weight supported treadmill training (BWSTT) on
muscle and bone in individuals with spinal cord injury (SCI). Fourteen individuals who sustained an incomplete SCI
at least 12 months before the study were recruited to participate in BWSTT 3 times/week for a total of 144 sessions.
Thirteen individuals completed the study. The average age of subjects was 29 y, average time post-injury was 7.70 y
(range: 124 y). Areal bone densities of the proximal and distal femur, proximal tibia, spine, and whole body were
measured using dual-energy X-ray absorptiometry. Muscle cross-sectional area (CSA), volumetric bone density, and
bone geometry at mid-femur and proximal tibia were measured using computed tomography. Serum osteocalcin and
urinary deoxypyridinoline were measured at baseline and after 6 and 12 months of training. All other measures were
made before and after training. Participants experienced significant increases in whole-body lean mass, from 45.9
8.7 kg to 47.8 8.9 kg (mean SD; p < 0.003). Muscle CSAs increased by an average of 4.9% and 8.2% at the thigh
and lower leg sites, respectively. No significant changes occurred in bone density or bone geometry at any site, or in
bone biochemical markers. Whole-body bone density exhibited a small but statistically significant decrease (p < 0.006).
BWSTT may therefore be a promising intervention for increasing muscle mass. Although 12 months of BWSTT did
not increase bone density in individuals with chronic incomplete SCI, it did not appear to decrease bone density at
fracture-prone sites.
Key words: spinal cord injury, bone density, muscle mass, osteoporosis, body weight support.
Rsum : Le but du cet tude tais analyser leffet dun entranement sur tapis roulant, dune dure de douze mois,
sur les os et les muscles de personnes prsentant une lsion mdullaire (SCI) et dont le poids corporel est support au
cours de lexercice (BWSTT). Quatorze individus atteints dune lsion incomplte de la moelle pinire au moins 12
mois prcdant ltude participent des sances dentranement raison de 3 sances par semaine pour un total de 144
sances. Treize sujets se rendent au bout du programme; leur ge moyen est de 29 ans et leur accident mdullaire remonte en moyenne 7,70 ans (cart de 1 24 ans). Les variables dpendantes sont t densit osseuse mesure au niveau des coupes proximale et distale du fmur, de la coupe proximale du tibia, de la colonne vertbrale et de tout le
corps par absorptiomtrie rayons X en double nergie. La surface de section transversale du muscle (CSA), la densit
volumtrique de los et la gomtrie de los la mi-longueur du fmur et au niveau proximal du tibia sont mesures
par tomographie assiste par ordinateur. Les concentrations sriques dostocalcine et urinaires de dsoxypyridinoline
sont mesures au dbut et aprs 6 et 12 mois dentranement. Toutes les autres mesures sont prises avant et aprs le
programme dentranement. On observe une amlioration significative de la masse maigre totale, soit 45,9 kg 8,7
47,8 kg 8,9 (moyenne -t; p < 0,003). La CSA augmente en moyenne de 4,9 % et 8,2 % la cuisse et la jambe,
respectivement. Cependant on nobserve, tous les endroits mesures, aucune variation significative de la densit osseuse et de la gomtrie osseuse ni des marqueurs biochimiques des os. tous les endroits mesurs. La densit osseuse
globale diminue un peu mais de faon significative (p < 0,006). Pour accrotre la masse musculaire, lapproche par
Received 19 May 2005. Accepted 29 November 2005. Published on the NRC Research Press Web site at http://apnm.nrc.ca
on 5 May 2006.
L.M. Giangregorio.1 Department of Kinesiology, University of Waterloo, 200 University Ave. West, Waterloo, ON N2L 3G1,
Canada; Spinal Cord Rehabilitation Program, Toronto Rehabilitation Institute, Toronto, ON, Canada; Department of Kinesiology,
McMaster University, Hamilton, ON, Canada.
C.E. Webber. Department of Nuclear Medicine, Hamilton Health Sciences, Canada.
S.M. Phillips, A.L. Hicks, and N. McCartney. Department of Kinesiology, McMaster University, Canada.
B.C. Craven. Spinal Cord Rehabilitation Program, Toronto Rehabilitation Institute, and Department of Medicine, University of
Toronto, Toronto, ON, Canada.
J.M. Bugaresti. Department of Medicine, McMaster University, Canada.
1

Corresponding author (e-mail: lmgiangr@healthy.uwaterloo.ca).

Appl. Physiol. Nutr. Metab. 31: 283291 (2006)

doi:10.1139/H05-036

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BWSTT semble prometteuse. Mme si douze mois dentranement nont pas amlior la densit osseuse chez des individus prsentant une lsion mdullaire incomplte chronique, on ne note aucune rduction de la densit osseuse aux
endroits plus sensibles aux fractures.
Mots cls : lsion mdullaire, densit osseuse, masse musculaire, ostoporose, support du poids corporel.
[Traduit par la Rdaction]

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Giangregorio et al.

Introduction
After spinal cord injury (SCI), there is a significant loss of
lower-limb bone density and muscle mass (Wilmet et al.
1995). Decreases in bone mineral density predispose individuals with SCI to an increased risk of fracture. Lower-limb
fractures in individuals with SCI are often a result of trivial
injuries or falls that would not normally cause a fracture,
demonstrating the severity of osteoporosis after SCI (Ingram
et al. 1989). Individuals with incomplete SCI tend to lose
less bone than individuals with complete SCI (Demirel et al.
1998; Garland and Adkins 2001; Sabo et al. 2001). Increased fat mass and muscle atrophy may predispose individuals with SCI to an increased risk for cardiovascular
disease, owing to a myriad of factors including reduced insulin sensitivity (Bauman and Spungen 1994).
Rehabilitation techniques, such as functional electrical
stimulation (FES), have been used to increase or prevent the
loss of bone and muscle in individuals with SCI. The ability
of FES to increase lower-limb muscle area in individuals
with SCI has been well documented (Belanger et al. 2000;
Dudley et al. 1999; Pacy et al. 1988; Scremin et al. 1999),
but the effects of FES exercise on the skeleton are not as
well established. Several studies have demonstrated no effect
of FES strengthening or cycle ergometry on bone mineral
density (BMD) (BeDell et al. 1996b; Bloomfield et al. 1996;
Eser et al. 2003; Leeds et al. 1990; Pacy et al. 1988),
whereas others have demonstrated increases in BMD after
resistance training with FES (Belanger et al. 2000) and FES
cycle ergometry (Mohr et al. 1997). The data on passive
standing or walking interventions in chronic SCI are limited,
and are generally restricted to effects on bone, not on muscle. A walking intervention for 1220 weeks, incorporating
an ambulation device that combined FES and a modified
walker, did not result in increased hip BMD (NeedhamShropshire et al. 1997). Regular standing with the use of a
standing frame did not increase BMD in chronic SCI, but
the average duration of the intervention was only 135 days
(Kunkel et al. 1993).
Body weight supported treadmill training (BWSTT) has
been applied recently for the rehabilitation of gait in individuals with incomplete SCI. Individuals with SCI who train
with BWSTT have demonstrated improvements in treadmill
speed and exercise duration, and some have shown functional improvements in their ambulatory abilities (Hicks et
al. 2002, 2005; Wernig et al. 1995). Stewart and colleagues
reported increases in muscle fibre size and a shift of the
fibre types toward a less-fatiguable fibre-type profile after
68 sessions, or approximately 6 months of BWSTT 3 times/
week (Stewart et al. 2004). Since BWSTT involves progressive mechanical loading of the limbs while individuals walk
on a treadmill, it was hypothesized that BWSTT might

291

improve bone mass and partially reverse muscle atrophy in

individuals with chronic, incomplete SCI. The current study
reports the impact of 144 sessions of BWSTT on bone and
muscle in individuals with SCI.

Materials and methods

Participants
The study was approved by the local Research Ethics
Board of Hamilton Health Sciences. Participants were recruited through contact with medical staff at The Central
Ontario West Regional SCI Rehabilitation Program at
Chedoke Hospital, Hamilton, and through local advertisements. Eleven males and 3 females agreed to participate,and
provided informed written consent. All participants had sustained a traumatic incomplete SCI at least 12 months before
entering the study, and all but 2 had some motor function, as
indicated by an American Spinal Injury Association (ASIA)
classification of C (Ditunno, Jr. et al. 1994). Participants
agreed to engage in BWSTT 3 times/week for a total of 144
sessions delivered over approximately 12 months, and had
received medical clearance from their physicians. The age,
gender, lesion levels, ASIA scores, and years post-injury of
the 14 participants are presented in Table 1. Exclusion criteria were as follows: cardiac pacemaker or documented heart
disease, uncontrolled cardiac dysrhythmia, chronic obstructive pulmonary disease, uncontrolled autonomic dysreflexia,
recent non-traumatic fracture, tracheostomy, bilateral hip
and knee flexion contractures greater than 20, drug addiction, age > 60 y or persons > 40 y who failed phase 1 of a
progressive incremental exercise tolerance test, severe muscle shortening, or severe skin ulcerations.
Four additional individuals (Table 2) originally recruited
to participate were not able to commit to BWSTT 3 times/
week for 12 months, and were subsequently included to provide a reference control group for the degree of variation of
bone and muscle over 1 year. After 6 months, 1 subject in
the reference control group was no longer able to return for
testing for personal reasons. All participants were instructed
to maintain current physical activity levels. For ethical reasons, participants who were taking osteoporosis medications
were not asked to discontinue them. Four of the 14 BWSTT
participants were taking a bisphosphonate. One of 3 reference group participants was taking a bisphosphonate at the
time of recruitment.
Intervention: body weight supported treadmill training
(BWSTT)
The Woodway Loco-System (Woodway USA Inc.,
Waukesha, Wis.) is a treadmill with an accompanying suspension system. Weight stacks that are attached to cables
can be used to provide graded vertical support for an
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Table 1. Descriptive characteristics of BWSTT participants.

Participant

Sex

Age

Lesion level

ASIA score

1
2
3
4
5
6
7
8
9
10
11*
12
13
14

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

31
22
32
22
26
24
28
33
53
20
27
29
24
32

C4
T12
C5/6
C5
T8
C5
C4
C4
C5
C5
C5
C5
C5
T12

C
C
C
C
C
C
C
C
C
C
C
B
C
B

No. of years post-injury

1.2
1.3
15
3.5
1.7
24
3.3
10
14
5
11
7
9
1.5

Note: C, cervical spine; T, thoracic spine.

*Participant did not complete the study.

Table 2. Descriptive characteristics of reference controls.

Subject

Sex

Age

Lesion level

ASIA score

1CN
2CN
3CN*
4CN

M
M
M
M

32
41
39
40

T12
C56
C8
C5

D
B
D
B

No. of years post-injury

3
24
13
25

Note: CN, control; C, cervical spine; T, thoracic spine.

*Participant did not complete the study.

individual to stand on the treadmill. Participants are fitted

into a specialized harness while seated, and the harness is
secured to overhead cables. During the first training session,
a level of body weight support (BWS) was chosen for each
participant so that they could maintain an upright trunk and
so that their knees would not buckle in quiet standing. If
BWS was set too low, participants tended to sit in the harness, which did not facilitate proper gait. The treadmilltraining strategy focused on proper weight shifting and
weight bearing during the loading phase, as well as maintenance of an upright torso. The initial sessions comprised
walking bouts of 515 min duration. Walking duration during each bout was increased gradually according to the participants tolerance. Most participants began training with
60% BWS or greater walking at treadmill speeds of
0.6 km/h or less. Over the course of training, both %BWS
and treadmill speed were modified on an individual basis to
increase training intensity, following the strategy of first unloading a portion of the BWS, then increasing treadmill
speed at each level of BWS. The maximum number of walking bouts per training session was 3. Trained kinesiology
and physiotherapy students assisted in BWSTT. One stood
behind the participant to provide trunk support and help initiate weight shifting, and the other 2 were positioned beside
the lower limbs to assist with stepping and limb control.
Outcome measures
Walking duration, walking speed, and amount of BWS
provided were recorded after each training session. A modified version of a scale developed by Wernig and collegues

(Wernig et al. 1995, 1998) was used to evaluate over-ground

walking abilities at each 3 month time point.
Bone mineral density (BMD), bone biochemical
markers, muscle mass, muscle cross-sectional area
Dual-energy X-ray absorptiometry (DXA; Hologic 4500A
densitometer, Bedford, Mass.) scans were performed at baseline and after training cessation to obtain areal bone mineral
density (aBMD, g/cm2) measurements of the lumbar spine
(L1L4 aBMD), right and left proximal femora (total hip
aBMD), and right distal femur and right proximal tibia (both
total aBMD). A whole-body scan was performed to measure
whole-body BMD, as well as muscle and fat masses. The
coefficient of variation for the lumbar spine quality-control
phantom during the period of the study was 0.52%. The
long-term precision for whole-body BMD using our equipment is 0.009 g/cm2. The proximal femur, lumbar, and
whole-body scans were analyzed using commercially available software from Hologic. Distal femur and proximal tibia
scans were analyzed using a modified lumbar spine protocol,
as described previously (Moreno 2001).
First morning urine and venous blood samples were taken
at baseline, and after 72 and 144 training sessions to assess
changes in urinary deoxypyridinoline (DPD) and serum
osteocalcin (OC). Serum and urine aliquots were stored at
80 C for later analysis. Urinary DPD and serum OC were
analyzed using competitive enzyme immunoassays (Quidel
Corporation, San Diego, Calif.). All samples were processed
in duplicate. Urinary DPD data were corrected for urinary
creatinine concentration, determined by a modified Jaffe
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Fig. 1. Amount of body weight support (BWS) and walking duration per bout at baseline and after 6 and 12 months of training.
100
90

Baseline
6 Months
12 Months

80

80

70

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60

60

50
40

40
30

20

20

Walking Duration per bout (min)

100

10
0

0
% BWS

method (Bowers and Wong, 1980). All analyses were conducted in the Exercise and Metabolism Research Group
Laboratory at McMaster University (Hamilton, Ont.).
A General Electric (GE) CTI Scanner (GE, Milwaukee,
Wis.) was used to perform computed tomography (CT) scans
at baseline and after cessation of training. A scout scan was
taken of the lower limbs to determine the femur and tibia
lengths and a helical scan was taken from mid-femur to midtibia. Mid-femur was defined as the midpoint between the
head of the femur and the medial joint line of the knee. Midtibia was defined as the midpoint between the medial tibial
plateau and the lateral malleolus. Slices used for analysis
were the mid-femur slice and the slice at the point of maximal lower-limb muscle cross-sectional area (CSA), defined
to be 66% of the tibia length (66% tibia), starting from the
distal end and measuring proximally. To ensure accurate positioning before and after training, the tibial plateau was
used as an anatomical landmark, and the slice containing it
was identified. Differences in leg length or differences in leg
positioning between baseline and post-training could be corrected for based on differences in the slice containing the
left and right tibial plateaus in each scan. The system parameters used were as follows: slice thickness, 5 mm; pixel
matrix, 512 512; exposure factors of 120 kV and 200 mA;
standard reconstruction algorithm.
Muscle CSAs were assessed at mid-femur and 66% tibia
sites. CT scans were analyzed using a validated software
program (BonAlyse 1.3, BonAlyse Oy, Jyvaskyla, Finland).
Thresholds of 270 to 101 Hounsfield units (HU) were
used to identify fat, and thresholds of 101 to 270 HU were
used to identify muscle. BonAlyse was also used to calculate
bone CSA (mm2) and volumetric BMD (vBMD, mg/cm3) at
mid-femur and 66% tibia. Thresholds for outer and inner
borders of bone were 280 and 70 mg/cm3, respectively.
Maximum (Imax) and minimum (Imin) cross-sectional moments of inertia and the polar cross-sectional moment of inertia (Ipolar) were calculated for femur and tibia slices. We

Duration

have determined that muscle and bone variables obtained

from CT scans using our scanner can be measured with
reproducibility, as assessed via the root mean squared coefficient of variation (Gluer et al. 1995), of less than 2% for
area and density variables and less than 2.6% for moment of
inertia variables. For both thigh and lower-leg sites, values
obtained for the right and left legs were averaged for each
variable in each participant.
Design and statistical analyses
A longitudinal, prospective, within-subject design was
used in which participants completed 144 sessions of
BWSTT over a period of 1215 months. The effects of the
intervention on bone and muscle outcome variables were assessed using multiple analyses of variance (MANOVA) for
repeated measures. Variables were analyzed in groups according to measurement technique. Densitometry data were
further subdivided by measurement site such that hip data,
lumbar spine data, whole-body data, proximal and distal
femur data, and proximal tibia data were all analyzed separately. CT muscle data was analyzed separately from CT
bone data. If a MANOVA was significant at p < 0.05, then
variables were individually contrasted using a Students t
test. DXA scan results were also normalized to T scores
using normative values provided with Hologic QDR 4500A
software, to present the skeletal status of participants relative
to normative data. Because there were only 3 individuals in
the reference control group, their data is reported, but statistical analyses were not performed.

Results
Adherence and adverse events
Participants were considered adherent with the intervention if they were able to complete the required 144 sessions
in a maximum of 15 months. One female subject (No. 11)
was not able to maintain the attendance requirement and did
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Treadmill and over-ground walking abilities

At baseline, all participants required some assistance with
at least one leg, if not both, during BWSTT. The impact of
BWSTT on ambulation in this group is reported elsewhere
(Hicks et al. 2005). Of 13 participants, 4 improved their
walking abilities on the Modified Wernig Scale by at least 2
points, and 1 person improved by a single point. The amount
of BWS required during BWSTT decreased progressively
with training (Fig. 1). All participants were able to progressively increase the speed at which they walked on the treadmill during training, and the total duration of walking per
bout.
Bone mineral density, body composition, and bone
biochemical markers
Applying the World Health Organization criteria for
osteoporosis to baseline hip BMD T scores, 8 participants
would have been considered osteoporotic at one or both
femora, 3 would have been osteopenic, and 2 would have
been considered to have normal BMD. Of 10 participants in
whom lumbar spine BMD measurements were possible, 4
participants would have been considered osteopenic at the
lumbar spine based on their T scores. All others had spine
BMD values within the normal range. There were no statistically significant changes in BMDs at proximal femur, lumbar spine, proximal tibia, or distal femur after BWSTT. The
interindividual variability in the BMD response to BWSTT
was large (Fig. 2). Differential responses to BWSTT did not
appear to be related to the amount of BWS required. However, when BMDs were examined on an individual basis,
changes in distal femur BMD were positive in all 8 subjects
except for 1, whose change was 11%. Coincidentally, this
individual was fewer than 2 y post-injury, whereas the remaining individuals in the group with distal femur BMD
measurements were greater than 2 y post-injury. Similarly, 4
individuals experienced reductions in average proximal
femur BMD that were greater than 3%, and 3 of these 4
individuals were fewer than 2 y post-injury at baseline.
The impact of BWSTT on body composition was significant
(p 0.05). There was a small, but statistically significant,
reduction in whole-body BMD (1.118 0.1 vs. 1.094
0.1 g/cm2, p = 0.006). In contrast, whole-body lean mass
exhibited a significant increase after 144 sessions of
BWSTT (45.9 8.7 kg vs. 47.8 8.9 kg, p = 0.003; Fig. 4),
with no significant change in whole-body fat mass (23.6

Fig. 2. Percent change in proximal femur BMD after BWSTT

intervention. Participants marked with a grey box are those who
were fewer than 2 years post-injury at baseline. Participant 11
did not complete the intervention.
10

%Change in BMD

not return for subsequent assessments. Average ( SD)

adherence during the BWSTT study was 78.7% 7.5%
(adherence = no. of sessions completed/total possible sessions 100%). The average number of sessions completed
per week was 2.4 0.2. Few adverse events were reported.
One individual experienced a pressure sore and returned to
training 3 times/week after it healed. Another individual experienced knee pain occasionally during training, and the
amount of BWS was increased and the session duration was
reduced temporarily to relieve the pain. Participants anecdotally
reported that regular BWSTT resulted in decreased lower
limb edema, reduced levels of spasticity, and produced a
feeling of warmth in the feet. One participant reported discontinued use of support stockings.

287

-10

-20
1

10

Participants
Fig. 3. Percent change in distal femur and proximal tibia BMD
after the BWSTT intervention. Participant 14 was fewer than
2 years post-injury at baseline. Distal femur and proximal tibia
scans could not be performed in participants 15. Participant 11
did not complete the intervention.
20

% Change in BMD

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Giangregorio et al.

10

0
10

Participants
-10

-20

Distal Femur
Proximal Tibia

11.0 kg vs. 24.0 10.6 kg). When the whole-body scan was
divided into upper and lower body, the increases in lowerbody lean mass that occurred after BWSTT were significant
(p 0.05), and the increases in upper-body lean mass
approached significance (p = 0.06).
Biochemical analyses were performed for 12 participants,
with 1 missing sample at the 72 session time point. OC
levels were at the high end of the normal range at baseline
and throughout the study, where normal levels are considered to be between 3.7 and 10.0 ng/mL for females and
between 3.4 and 9.1 ng/mL for males. DPD levels were approximately 23 times higher than normal (where normal is
3.07.4 nmol DPD/mmol Cr for females, 2.35.4 nmol
DPD/mmol Cr for males) at baseline and throughout the
study; mean ( SD) levels were 13.8 18.1 nmol
DPD/mmol creatinine at baseline, and 14.8 23.4 and 12.5
15.3 nmol DPD/mmol creatinine after 72 and 144 sessions
of BWSTT, respectively. Levels of both biochemical markers
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Appl. Physiol. Nutr. Metab. Vol. 31, 2006

Fig. 4. Percent changes in lean mass, fat mass, and muscle cross-sectional area after BWSTT. Mean % changes are indicated within
each box, with statistically significant increases denoted by an asterisk. Black dots indicate outliers.
50

40

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30

20

10
4.4%*

5.1%

4.9%*

Whole Body
Fat Mass

Thigh
Muscle CSA

8.2%*

-10

-20
Whole Body
Lean Mass

were not significantly different from baseline at any time

during BWSTT.
Muscle cross-sectional area (CSA) and bone density
and geometry measured with computed tomography
Significant increases in thigh and calf muscle CSA (mm2)
occurred after 144 sessions of BWSTT (p 0.05, Fig. 4).
The average increases in muscle CSA at mid-thigh and calf
(66% tibia length) sites were 4.9% 7.6% and 8.2%
9.0%, respectively (Table 5). There were no significant
changes in bone geometry or volumetric BMD at mid-femur
and 66% tibia sites after BWSTT (Table 3).
Reference control group
Proximal femur BMD was reduced in 1 control participant
(right, 2.7%; left, 10%), but not in the others. Two control
participants experienced reductions in proximal tibia BMD,
and all 3 experienced reductions in distal femur BMD, ranging from 0.9% to 8.6%, whereas 1 of 8 participants in the
BWSTT group experienced an appreciable loss in distal
femur BMD (11%). All individuals in the reference control
group experienced reductions in thigh and lower limb muscle
CSA, ranging from 2.3% to 16.8%.

Discussion
The current study represents the first prospective, longitudinal study evaluating the effects of 1 y of BWSTT on walking abilities, bone, and muscle in individuals with chronic
incomplete SCI.
Effects of BWSTT on the skeleton
BWSTT performed three times per week did not appear to
have a demonstrable effect on the skeleton in these individu-

Calf
Muscle CSA

als with SCI. We did note a small, but statistically significant, decrease in whole-body BMD; however, considering
the magnitude of the change and the absence of change at
standard sites used to assess fracture risk (e.g., proximal
femur) this decrease does not necessarily indicate increased
risk. There may be specific factors that determine if BWSTT
can positively impact the skeleton (e.g., age, length of time
after injury, level of injury). For example, 3 of 4 individuals
who experienced reductions in average proximal femur
BMD greater than 3% were fewer than 2 years post-injury at
baseline. These individuals were likely still experiencing
accelerated bone mineral loss as a result of SCI, and
BWSTT did not completely prevent that loss. Similarly, at
the distal femur, when 1 individual who was only 1 postinjury at baseline was excluded, BMD either remained stable
or increased in the remaining participants. It is possible that
BWSTT may prevent further bone loss and can increase
BMD in some people, but the large inter-individual variation
makes it difficult to draw firm conclusions.
A few other, shorter-duration studies have examined the
impact of walking or standing interventions on bone in individuals with chronic SCI, and did not demonstrate increases
in BMD following the intervention (Needham-Shropshire et
al. 1997; Kunkel et al. 1993). Other studies suggest that
weight-bearing interventions may need to be initiated in the
acute stages after SCI to realize any positive skeletal effects
(Goemaere et al. 1994; de Bruin et al. 1999). Several studies
have demonstrated that FES-based interventions do not increase lower-limb BMD in individuals with SCI (BeDell et
al. 1996a; Bloomfield et al. 1996; Leeds et al. 1990; Pacy et
al. 1988). Two FES studies that demonstrated increases in
BMD in individuals with chronic, complete SCI were of
longer duration than most studies, and 1 incorporated FES
exercise 5 d/week (Belanger et al. 2000; Mohr et al. 1997).
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Table 3. Mean bone density and bone geometry at mid-thigh and lower leg before and after BWSTT.

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Mid-femur
Pre-BWSTT
Post-BWSTT
Lower leg
Pre-BWSTT
Post-BWSTT

CSA
(mm2)

BMD
(g/cm3)

BMC (g)

Imax

Imin

Ipolar

Cortical CSA
(mm2)

Cortical BMD
(g/cm3)

434.587.9
429.082.9

770.489.0
758.185.2

1673.9394.7
1626363.8

3124010425
3115510382

23100881
23069883

5434118791
5410218725

361.898.1
353.089.8

847.948.4
840.943.4

387.066.8
381.363.0

745.087.8
727.871.4

1437.3281.9
1384.2251.1

3704111414
3631210382

16840557
16712553

5388016288
5302414928

297.067.5
291.060.2

851.356.4
834.238.0

Note: Data are presented as mean SD.

Effects of BWSTT on muscle

Application of BWSTT was effective for increasing muscle area in individuals with SCI, as measured by CT and
DXA. The noted increases in thigh muscle CSA of approximately 5% are smaller than those reported for FES interventions (Dudley et al. 1999; Skold et al. 2002). The differences
may be attributable to intensity; the muscle activity achieved
with FES is likely larger than could be achieved during
BWSTT. However the pattern of muscle fibre activation
achieved via FES is not physiological. Increases in muscle
CSA as a result of BWSTT are particularly relevant in light
of the decreases in muscle CSA, ranging from 2.3% to
16.8%, seen in the reference group. In a sub-group of participants who underwent muscle biopsies, approximately
6 months of BWSTT resulted in significant increases in
mean muscle fibre area of 25.5% 6.3% (Stewart et al.
2004). In addition, there was an increase in the proportion of
type IIa fibres and a reduction in type IIax/IIx fibres. These
data further support the idea that BWSTT results in muscle
growth and positive changes in muscle morphology in atrophied muscles of individuals with incomplete SCI.

Most studies concur that functional improvements in

walking with BWSTT can only be achieved in individuals
with incomplete lesions, suggesting that other factors are important for attainment of over-ground walking. In support of
this thesis, when we evaluated the improvements in our
study on a case-by-case basis, it was evident that the level of
baseline motor function may have dictated if walking abilities learned on the treadmill could be transferred to overground walking. Individuals who experienced the largest
improvements in walking abilities and achieved over-ground
walking had the greatest lower-extremity motor function at
baseline, defined as an ability to stand independently, or take
a few steps using assistive devices. Individuals who had little
motor function made much smaller improvements on the
treadmill, and could not walk over ground after BWSTT
training, with or without assistive devices. The regular
BWSTT could be a stimulus that improves muscle mass and
function and reduces fatigueability. In fact, the largest
changes in muscle CSAs were noted in individuals who
made the greatest improvements in over-ground walking. As
well, BWSTT results in increases in muscle fibre size and a
shift of fibre types toward a less-fatigueable fibre-type profile after only 68 training sessions (Stewart et al. 2004).
We did not exclude participants based on their potential to
use assistive devices. In the work by Wernig et al. (1995),
participants were trained once or twice per day, 5 d/week, in
a residential hospital. Participants were required to have
some voluntary activity in lower-limb muscles and a reasonable potential to use canes or other assistive devices (Wernig
et al. 1995). It is possible that the training intensity and selection of patients explains why those researchers observed
such dramatic changes in walking abilities, whereas we did
not. Given that our participants could not maintain attendance at a frequency of 3 times/week, it is likely that a prescription of BWSTT 5 times/week may be impractical in an
outpatient rehabilitation setting.

Effects of BWSTT on walking abilities

Earlier work using BWSTT examined the effects of shortterm training, and suggested that BWSTT could dramatically
improve the walking abilities of wheelchair-bound individuals (Dietz et al. 1994, 1995; Wernig et al. 1995) and that,
with locomotor training, the human spinal cord can produce
electromyographic activity resembling that observed during
locomotion (Dietz et al. 1994, 1995; Harkema et al. 1997;
Pinter and Dimitrijevic 1999; Wirz et al. 2001). Wernig et al.
(1995) also demonstrated that improved capacity for independent stepping was not necessarily associated with an
increase in voluntary muscle activity.

Limitations and future directions

A randomized, controlled design was not employed owing
to the small number of subjects recruited and the high potential for drop out among subjects who would be randomized
to the control group. Even with a larger number of participants, it would have been difficult to establish adequate
matching between control and intervention groups owing to
inter-individual variability in characteristics such as age,
gender, level of lesion, ASIA score, and time post-injury.
The inclusion criteria for future BWSTT studies should be
appropriate to the outcomes of interest. For example, studies
looking at the impact of BWSTT on bone should include

It is possible that potential for recovery of lost bone after

SCI is minimal, or that the applied strain rate and (or) strain
magnitude associated with BWSTT was insufficient for increasing BMD (Frost 1987). Most participants still required
some BWS after 144 sessions, and most walking speeds
were below what would be considered normal for able-bodied
individuals. The intensity of BWSTT is largely determined
by an individuals capabilities, thus predetermined training
intensities consistent across subjects cannot be incorporated.
The frequency of exercise may also not have been sufficient
to be osteogenic; average attendance was 2.4 0.2 times/
week. In accordance with recent animal research, shorter,
more frequent exercise bouts may be the best strategy for increasing bone mineral accretion (Robling et al. 2002).

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individuals that are at a common phase post-injury (either

>2 or 3 y post-injury or in the acute stages). Furthermore, it
may not be ethical to exclude participants because they are
not likely to make improvements in walking abilities, since
we have demonstrated that even in the absence of dramatic
changes in walking abilities, BWSTT can increase lean mass.
As well, improvements in outcomes that are relevant to
patients (e.g., spasticity) were anecdotally reported, and
should be examined further.
Summary
BWSTT performed 3 times/week for approximately
12 months had a significant impact on whole-body and
lower-limb lean mass and muscle CSA in individuals with
chronic incomplete SCI. Individuals participating in BWSTT
improved their walking abilities on the treadmill, and a few
individuals improved their over-ground walking abilities.
BWSTT did not appear to improve BMD in the group as a
whole; however, when evaluated in a case-by-case basis,
BMD at fracture-prone sites tended to remain stable or
increase in most individuals who were more than 2 postinjury. Multi-centre trials are required to confirm the effectiveness of BWSTT as a gait-retraining intervention, and to
further elucidate its impact on important health outcomes.

Acknowledgements
The study was completed using a grant from the Ontario
Neurotrauma Foundation awarded to N.M. and colleagues. L.G. was the recipient of a Health Research Partnership Fellowship Award from the Ontario March of Dimes
and the Canadian Institutes of Health Research. We also
express sincere thanks to Megan Smith, Leslie Radforth,
Howard Hollingham, and all the volunteer trainers and the
study participants for their dedication to this research.

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