Effects of whole-body vibration on blood flow and neuromuscular activity in spinal cord injury

Abstract

Crossover trial.
To investigate the effects of whole-body vibration (WBV) on muscular activity and blood flow velocity after different vibration treatments in patients with spinal cord injury (SCI).
Research Center on Physical Disability (Spain).
Eight individuals with SCI received six 3-min WBV treatments depending on a combination of frequency (10, 20 or 30 Hz) and protocol (constant, that is, three consecutive minutes of WBV, or fragmented, that is, three sets of 1 min of WBV with 1 min of rest between the sets). Femoral artery blood flow velocity was registered at minutes 1, 2 and 3 of WBV, and at minutes 1 and 2 after the end of the stimulus. Electromyography activity (EMG) of vastus lateralis (VL) and vastus medialis (VM) was registered at baseline and during WBV.
Peak blood velocity (PBV) increased after 1, 2 and 3 min of WBV. The 10 Hz frequency did not alter blood flow, whereas the 20 Hz frequency increased PBV after 2 and 3 min of WBV, and the 30 Hz frequency increased PBV after 1, 2 and 3 min of WBV and during the first minute after the end of the stimulus. No protocol effect was observed for blood parameters. EMG activity of VL and VM increased independently of the applied frequency or protocol.
WBV is an effective method to increase leg blood flow and to activate muscle mass in SCI patients, and could be considered to be incorporated in their rehabilitation programs.

Full text

UNCORRECTED PROOF
ORIGINAL ARTICLE
Effects of whole-body vibration on blood flow and neuromuscular
activity in spinal cord injury
AJ Herrero
1,2
, H Mene
´ndez
1
, L Gil
1
, J Martı
´n
1
, T Martı
´n
1
, D Garcı
´a-Lo
´pez
2
,A
´Gil-Agudo
3
and PJ Marı
´n
1,2
1
Research Center on Physical Disability, ASPAYM Castilla y Leo
´n, Valladolid, Spain;
2
Laboratory of Physiology, Faculty of Health
Sciences, Miguel de Cervantes European University, Valladolid, Spain and
3
Biomechanics and Technical Aids Unit, Physical Medicine
and Rehabilitation Department, National Hospital for Spinal Cord Injury, SESCAM, Toledo, Spain
Study design: Crossover trial.
Objectives: To investigate the effects of whole-body vibration (WBV) on muscular activity and blood
flow velocity after different vibration treatments in patients with spinal cord injury (SCI).
Setting: Research Center on Physical Disability (Spain).
Methods: Eight individuals with SCI received six 3-min WBV treatments depending on a combination
of frequency (10, 20 or 30 Hz) and protocol (constant, that is, three consecutive minutes of WBV, or
fragmented, that is, three sets of 1 min of WBV with 1 min of rest between the sets). Femoral artery
blood flow velocity was registered at minutes 1, 2 and 3 of WBV, and at minutes 1 and 2 after the end of
the stimulus. Electromyography activity (EMG) of vastus lateralis (VL) and vastus medialis (VM) was
registered at baseline and during WBV.
Results: Peak blood velocity (PBV) increased after 1, 2 and 3 min of WBV. The 10Hz frequency did not
alter blood flow, whereas the 20 Hz frequency increased PBV after 2 and 3 min of WBV, and the 30 Hz
frequency increased PBV after 1, 2 and 3 min of WBV and during the first minute after the end of the
stimulus. No protocol effect was observed for blood parameters. EMG activity of VL and VM increased
independently of the applied frequency or protocol.
Conclusion: WBV is an effective method to increase leg blood flow and to activate muscle mass in SCI
patients, and could be considered to be incorporated in their rehabilitation programs.
Spinal Cord (2010) 0, 000–000. doi:10.1038/sc.2010.151
Keywords: vibration frequency; oscillating platform; Doppler ultrasound; electromyography;
rehabilitation
Introduction
Spinal cord injury (SCI) has muscular and vascular con-
sequences below the level of the injury.
1
Regarding muscular
changes, these patients suffer a dramatic loss of muscle
mass.
2
Immediately after the injury and in the following
months, there is a preferential atrophy of type 2 fibers, but
past 7–10 months post injury, a significant shift of type 1
fibers to type 2B has been observed.
3
Regarding vascular
changes, there is a reduction in the thigh blood flow,
4
femoral artery diameter,
1
vascular reactivity,
1
and capillary
alterations.
3
It has been proposed that changes in the muscle
vascular function are parallel to the skeletal muscle atrophy
in SCI subjects,
1
and both changes increase the risk of
cardiovascular disease
5
and the development of pressure
ulcers.
6
Therefore, part of the rehabilitation of SCI patients
should focus on the activation of muscular and vascular
systems.
4
The application of whole-body vibration (WBV) with
platforms has been shown to improve muscular
7,8
and
vascular
9–11
functions. These effects are strongly dependent
on the type of platform, protocols and vibration parameters
(that is, frequency).
7
Specifically, greater vibration frequen-
cies induce higher-muscle activity
8
and greater blood flow
11
than lower frequencies. Moreover, the most common
protocol used to apply WBV consists of short bouts (30–
90 s) with B60 s rest between the sets. The effects induced by
the application of longer bouts (3 min) on peripheral
circulation have been poorly investigated.
The previously mentioned benefits of WBV have been
observed in healthy subjects; however, no study has focused
on the effects of WBV on the muscle and vascular responses
of SCI patients. Thus, the purpose of this study was to
investigate the effects of WBV on muscular activity and
blood flow velocity after different vibration treatments in
SCI patients.
Received 14 July 2010; revised 22 September 2010; accepted 28 September
2010
Correspondence: Dr AJ Herrero, Laboratory of Physiology, Faculty of Health
Sciences, Miguel de Cervantes European University, c/Padre Julio Chevalier,
Valladolid 47012, Spain.
E-mail: jaherrero@oficinas.aspaymcyl.org
Spinal Cord
(2010), 1–6
&
2010 International Spinal Cord Society All rights reserved 1362-4393/10
$
32.00
www.nature.com/sc

UNCORRECTED PROOF
Materials and methods
Subjects
Eight patients (six males and two females) volunteered to
participate in the study. All the patients had SCI and used
wheelchair for their locomotion. All the subjects were
classified as ASIA A
Q1 by the American Spinal Injury Associa-
tion.Table 1 summarizes the characteristics of the sample.
All the subjects received rehabilitation ten 2-h sessions per
month, which consisted of standing position (or tilt
position), passive movements, low intensity resistance
training or electrotherapy, and physiotherapy treatment.
Experimental treatments were applied to the subjects before
their rehabilitation routines. Subjects did not allow their
sleeping, eating and drinking habits to change throughout
study participation. We certify that all applicable institu-
tional and governmental regulations concerning the ethical
use of human volunteers were followed during the course of
this research.
Experimental design
Each subject was assessed in eight different sessions. In the
first two sessions, subjects were familiarized with the testing
treatments and vibration stimulus. Both sessions were
carried out within the same week separated with at least
48 h. The other six sessions were carried out on Monday,
Wednesday and Friday during the following two weeks. In
each session, a random WBV treatment was applied. The six
WBV treatments arise from the combination of the inde-
pendent variables frequency (10, 20 or 30 Hz) and protocol
(constant or fragmented). WBV was applied for three
consecutive minutes during the constant protocol
Q2 , whereas
three cycles of 1 min of WBV and 1min of resting period
were applied during the fragmented protocol (Figure 1).
Treatment protocol
Once a subject came to the laboratory, he or she was laid down
and fixed to a tilt table with straps (Figure 2). In the distal part
of the tilt table, just beneath the feet, a vibration platform was
placed (Galileo Home, Galileo, Novotec, Germany). Knee
angle was of 601flexion (considering 01the full knee
extension). Subsequently, the tilt table was placed at 451and
the subject was kept in that position for a period of 10 min
before the application of WBV. All the subjects were familiar-
ized with the tilt table and the chosen angle as they usually
maintain this position in their rehabilitation routines. In that
position, the subject was prepared to register electromyogra-
phy activity (EMG) and ultrasound variables. The frequency of
vibration was set at 10, 20 or 30 Hz. The amplitude of the
vibration was set by the position of the feet on the WBV plate
at 5 mm (peak– peak). Feet were placed paralle l to each other
38 cm apart (measured from the midlines of the feet). The
patients were exposed to the vibration each day for a total of
3 min continuous (constant) or fragmented (three bouts 60 s
exposures, separated by 60 s rests).
Ultrasound measurements
Blood parameters were registered through an ultrasound
system (MyLab 25, Esaote, Genoa, Italy) using a pulsed color
Doppler with a linear array transducer (LA 523, 7.5–12 MHz;
length, 50 mm; Esaote, Genua, Italy) in the femoral arter y as
previously described.
11
Blood parameters were analyzed at
baseline, at the end of minutes 1, 2 and 3 of WBV, and at the
end of minutes 1 and 2 of recovery after the stop of WBV
(Figure 1). Each image recorded by the ultrasound system
corresponded to a period of 4 s. In that period, there were
between 3 and 5 beats, and the mean of these beats was
analyzed to obtain: mean and peak systolic blood velocities
(MBV and PBV, respectively), as well as heart rate.
NP G _ S C _ SC 2 01 0151
Table 1 Descriptive characteristics of the study sample
Gender Age (years) Height (m) Mass (Kg) Years after injury Level of lesion ASIA score PBV (cm s
1
)
a
MBV (cm s
1
)
a
1 M 41 1.74 83 24 T5 A 80.4±8.4 36.5±3.7
2 M 32 1.85 80 4 T8 A 66.6±3.5 33.0±3.9
3 M 32 1.98 94 5 C6 A 47.5±6.8 25.1±5.1
4 M 39 1.87 82 3 T3 A 59.4±6.1 30.1±3.5
5 M 33 1.74 78 3 C6 A 82.2±7.7 35.7±4.4
6 M 32 1.73 76 2 C6 A 83.2±6.9 42.8±6.0
7 F 35 1.63 78 6 L1 A 49.2±4.1 26.2±3.5
8 F 45 1.71 70 22 C5 A 66.5±5.0 34.8±3.2
Mean 36.1 1.78 80.1 8.6
s.d. 5.0 0.11 6.9 9.0
Abbreviations: MBV, mean blood velocity; PBV, peak blood velocity.
a
Mean±s.d. of the control period values of the six sessions.
Figure 1 Sketch of the experimental phase in 10 s intervals showing the fragmented (top) and constant (bottom) protocols.
Electromyography (diamonds) and blood parameters (circles) were registered.
Whole body vibration in spinal cord injury
AJ Herrero et al
2
Spinal Cord

UNCORRECTED PROOF
Surface electromyographic activity
Muscle activity of the vastus medialis (VM) and vastus
lateralis (VL) was measured using EMG. One set (two
measuring electrodes) of surface electrodes (Ag/AgCl, Skin-
tact, Austria
Q3 ) was placed longitudinally to the direction of
the muscle fibers and approximately halfway from the motor
point area to the distal part of the muscle. An inter-electrode
distance of 2 cm was maintained. Before electrode place-
ment, the area was shaved, abraded and cleaned with
isopropyl alcohol in order to reduce skin impedance until
it was lower than 5 kO. The location of the electrodes on the
skin was marked with permanent ink in order to ensure the
same placement throughout the different sessions.
Myoelectric raw signals were detected with a two-channel
EMG device (MyoTrac Infiniti, Thought Technology, Mon-
tre
´al, Canada). EMG data analysis was performed with a
specific software (BioGraph Infiniti, Thought Technology,
Montre
´al, Canada). The last 10 s corresponding to the
control period and corresponding to the third minute of
WBV application were chosen for data analysis by the
aforementioned software (Figure 1). EMG raw data was
averaged by root mean square (EMG
RMS
) in order to obtain
the average amplitude of the EMG signal. On the basis
of the frequency analysis, a bandwidth of ±0.8 Hz around
each harmonic was excluded from the root mean square
calculation.
Statistical analysis
The normality of the dependent variables was checked and
subsequently confirmed using the Kolmogorov–Smirnov
test. A three-way repeated-measures analysis of variance in
frequency, protocol, and time was applied to analyze EMG
and blood parameters. When a significant F-value was
achieved, pair-wise comparisons were performed using the
Bonferroni post hoc procedure. The reliability and variability
of blood parameters were assessed with intraclass correlation
coefficient and coefficients of variation (that is,
CV ¼s.d.*100/mean). A paired t-test was used to analyze
differences between both basal values. Statistical significance
was set at Pp0.05. Effect size statistic, Z,
2
was analyzed to
determine the magnitude of the effect independent of
sample size. Values are expressed as mean±s.d.
Results
Blood parameters
Table 2 shows the statistical significance and effect sizes
of the analysis of variances. PBV increased after 1, 2 and
3 min of WBV (11.3±10.3%, Po0.05, 19.0±13.5% and
23.0±14.4%, Po0.01, respectively). At 1 and 2 min after
the stop of the stimulus, PBV decreased at minute 3 of WBV
(14.4±9.3% and 14.0±8.5%, Po0.05, respectively) and
Q4
was similar to baseline values. Regarding baseline values, the
10 Hz frequency did not modify PBV, whereas the 20 Hz
frequency increased PBV after 2 and 3 min of WBV, and the
30 Hz frequency increased PBV after 1, 2 and 3 min of WBV as
well as during the first minute after the end of the stimulus
(Figure 3).
MBV increased after 1, 2 and 3 min of WBV (22.0±10.1%,
31.1±11.0% and 36.0±12.7%, Po0.001, respectively). Like-
wise, MBV remained increased in respect to baseline 1 min
after the stop of the WBV (14.0±8.1%, Po0.05). The 30 Hz
frequency increased MBV more than the 10 Hz frequency
(26.8±8.1% in respect to 13.0±8.7%, Po0.001). However,
no differences were observed between the increment with
20 Hz (17.0±11.3%) and the other two frequencies. All the
frequencies increased the MBV in respect to baseline at
minutes 1, 2 and 3 of WBV (Figure 4). Furthermore, 30 Hz
NP G _ S C _ SC 2 01 0151
Figure 2 Placement of the subject on the tilt table during the
application of the whole-body vibration.
Table 2 Summary of the main effects analyzed with the ANOVAs for the dependent variables: PBV, MBV, HR, VM EMG
RMS
and VL EMG
RMS
Time Frequency Time*frequency Time*protocol
PBV ICC ¼0.962; CV ¼5.6 Po0.001; Z
2
¼0.567 NS Po0.001; Z
2
¼0.342 NS
MBV ICC ¼0.888; CV ¼8.4 Po0.001; Z
2
¼0.756 Po0.01; Z
2
¼0.403 Po0.01; Z
2
¼0.254 NS
HR ICC ¼0.973; CV ¼2.8 NS NS NS NS
VM EMG
RMS
Po0.05; Z
2
¼0.237 NS Po0.05; Z
2
¼0.321 Po0.05; Z
2
¼0.268
VL EMG
RMS
Po0.05; Z
2
¼0.268 NS Po0.01; Z
2
¼0.275 Po0.05; Z
2
¼0.293
Abbreviations: ANOVA, analysis of variance; CV, coefficient of variation; HR, heart rate; ICC, intraclass correlation coefficient; MBV, mean blood velocity; NS, non-
significant; PBV, peak blood velocity; VL EMG
RMS,
vastus lateralis EMG activity; VM EMG
RMS,
vastus medialis EMG activity.
For each effect, the statistical significance and effect sizes are shown. For the blood parameters, the ICC and CV are shown.
At the beginning and at the end of the control period, blood parameters were registered to analyze their reliability and to establish baseline level as the mean of
both values.
Whole body vibration in spinal cord injury
AJ Herrero et al
3
Spinal Cord

UNCORRECTED PROOF
increased MBV to a higher extent than 10 Hz and maintained
the MBV increased in respect to baseline values 1 min after
the end of the WBV. No protocol effect was observed for PBV
or MBV.
EMG
Regarding VM, EMG
RMS
was higher after 3 min of WBV in
respect to baseline values (26.0±9.9 in respect to
18.9±2.8 mV, Po0.05). Likewise, for each frequency,
EMG
RMS
was higher after 3 min of WBV in respect to
baseline values, but no differences in baseline values nor
after WBV were observed among frequencies. For both
protocols, EMG
RMS
was higher after 3 min of WBV in respect
to baseline values, no differences in baseline values were
observed between protocols, but after WBV, EMG
RMS
was
greater after the constant protocol (28.5±5.7 in respect to
23.5±3.3 mV, Po0.05).
Regarding the VL, EMG
RMS
was higher after 3 min of WBV
in respect to baseline values (26.2±5.8 in respect to
15.2±1.1 mV, Po0.05). For each frequency, EMG
RMS
was
higher after 3 min of WBV in respect to baseline values, but
no differences in baseline values nor after WBV were
observed among frequencies. Finally, for both protocols,
EMG
RMS
was higher after 3 min of WBV in respect to baseline
values, no differences in baseline values were observed
between protocols, but after WBV, EMG
RMS
was greater after
the constant protocol (29.7±7.5 in respect to 22.8±4.3 mV,
Po0.05).
Discussion
The main findings of the present study were that WBV alone
can significantly increase leg blood flow velocity and EMG
activity in SCI patients. Moreover, higher frequencies (that
is, 20 and 30 Hz) produced greater increase in leg blood flow
velocity, although a tendency to evoke higher increase in
blood flow velocity was observed with 30 Hz, which also
maintained this variable above basal values after the stop of
the stimulus. No difference was observed regarding the
application of the WBV in a constant or fragmented
protocol.
Leg blood flow velocity was increased during the applica-
tion of WBV in SCI patients. However, the magnitude of
blood flow response observed in our study is lower than in
others carried out with healthy subjects.
9,11
Using an
oscillating platform, Kerschan-Schindl
9
found a two-fold
increase in mean blood flow in the popliteal artery
and Lythgo et al.
11
found a four-fold increase in mean
blood velocity in the femoral artery. These greater responses
in comparison to our results could be due to the fact that:
(1) the tilt table provides weight unloading, and as blood
flow highly correlates with work output,
12
a reduction in
work output owing to unloaded weight may result in a
smaller increase in blood flow;
10
(2) greater the active tissue,
higher the metabolic demand; as muscle weakness is a
feature of SCI,
2
the O
2
demand should be reduced and
subsequently would elicit a reduced response; and (3) the
reduced femoral artery diameter and blood flow observed in
SCI patients
1
would limit the hemodynamic response
to exercise.
WBV leads to an increased metabolic demand measured by
oxygen uptake in a linear relationship with vibration
frequency,
13
which is in agreement with our results. As
higher the frequency used, the greater increase in blood flow
velocity was observed. Although there was no difference in
this variable between 20 and 30 Hz, a trend to produce
higher increase with 30 Hz was detected. Furthermore, 30 Hz
maintained the PBV above basal values 1 min after the stop
of the vibration. This would recommend using 30 Hz in order
to analyze the long-term effects of the application of WBV in
SCI patients.
To the best of our knowledge, this is the first study to apply
WBV on a tilt table on SCI patients. Other ways of applying
NP G _ S C _ SC 2 01 0151
-5
0
5
10
15
20
25
30
35
40
45
50
55
60
65
Changes on Mean Blood Velocity (%)
Time (s)
Whole body vibration
10 Hz
20 Hz
30 Hz
***
***
***
a
***
a
**
b
***
aaa
**
**
*** ***
B 60 120 180 240 300
Figure 4 Time course changes on mean blood velocity depending
on the frequency during and after the application of 3 min of whole-
body vibration and three cycles of 1 min of vibration and 1 min
resting period. **
,
*** different from baseline at Po0.01 and 0.001,
respectively.
a, aaa, b
different from 10 Hz at Po0.05, Po0.001 and
P¼0.08, respectively.
-5
0
5
10
15
20
25
30
35
40
45
50
Changes on Peak Blood Velocity (%)
Time (s)
Whole body vibration
10 Hz
20 Hz
30 Hz
**
**
**
**
a
**
**
aaa
B60
120 180 240 300
Figure 3 Time course changes on PBV depending on the frequency
during and after the application of 3min of whole-body vibration
and three cycles of 1 min of vibration and 1min of resting period.
** different from baseline at Po0.01.
a, aaa
different from 10 Hz at
Po0.05 and Po0.001, respectively.
Whole body vibration in spinal cord injury
AJ Herrero et al
4
Spinal Cord

UNCORRECTED PROOF
WBV on SCI patients have been through partial standing or
standing on the platform with the help of a specific device.
14
In the present study, the tilt table was fixed at an angle of 451
for the following reasons: (1) this angle unloads part of the
weight of the subject but less than a sitting position; (2) SCI
patients can experience episodes of orthostatic hypotension
and can faint if angles near to the vertical are reached
15
and
(3) all the participants were familiarized with this angle as
they used to maintain this position during 30 min in their
rehabilitation routines.
The improvement of lower-extremity circulation is a goal
of the rehabilitation of SCI patients.
4
Some of the traditional
exercises performed to achieve this goal have been passive
leg movements and passive cycling; however, there is
evidence supporting that these methods do not increase
leg blood flow in SCI patients.
16
As well as increasing
blood flow, the application of WBV during supine bed rest
for 52 days avoided a decrease of the diameter of the
common femoral artery in respect to a control group.
17
This
observation has not been reported in SCI patients but future
studies that combine WBV and Doppler ultrasound measures
should contrast if this preservation is possible in this
collective.
EMG
RMS
of VL and VM increased after the application of
WBV independently of frequency or protocol. In healthy
subjects, the same increases have been reported using
frequencies between 15 and 30 Hz.
18
In SCI patients,
we have not found any research that combines WBV and
EMG recordings, nevertheless the application of punctual
vibration on thigh muscles during locomotion increased the
muscle activity of SCI patients.
19
This increase in the
EMG
RMS
could be due to the fact that mechanical vibrations
applied to the muscle or tendon stimulate sensory
receptors and that activation of muscle spindles facilitates
the activation of a-motoneurons, leading to tonic vibration
reflex.
20
In our study, no significant difference was
noted depending on the frequency. It could be expected
that 30 Hz would increase EMG amplitude more than
10 Hz, as the acceleration of the platform is higher as the
frequency increases. Furthermore, in healthy subjects, great-
er EMG activity with high-frequency WBV training (40 and
45 Hz) has been reported when compared with lower
frequencies (25 and 30 Hz).
8
In our study, the lack of
differences in the EMG activity between frequencies could
be due to the reduced EMG response of SCI patients in
respect to healthy subjects,
21
as well as to the marked
difference in the EMG patterns among SCI subjects;
21
therefore, this lack of statistical significance could be due
to a type II error.
In conclusion, WBV represents an option to induce a reflex
muscle contraction in subjects with difficulties or inability to
evoke voluntary contractions such as SCI patients. Our
results show that WBV is an effective method to increase leg
blood flow and to activate muscle mass in these patients, and
could, therefore, be considered to be incorporated in
rehabilitation programs of this collective. Moreover, the
methodology proposed to apply SCI through the use of a tilt
table has been safe, easy to perform and welcomed by the
subjects and therapists.
Conflict of interest
The authors declare no conflict of interest.
Acknowledgements
This work was supported in part by a grant from the
IMSERSO (37/2008).
References
1 Olive JL, Dudley GA, McCully KK. Vascular remodeling after
spinal cord injury. Med Sci Sports Exerc 2003; 35: 901–907.
2 Giangregorio L, McCartney N. Bone loss and muscle atrophy in
spinal cord injury: epidemiology, fracture prediction, and
rehabilitation strategies. J Spinal Cord Med 2006; 29: 489–500.
3 Scelsi R. Skeletal muscle pathology after spinal cord injury: our 20
year experience and results on skeletal muscle changes in
paraplegics, related to functional rehabilitation. Basic Appl Myol
2001; 11: 75–85.
4 Nash MS, Montalvo BM, Applegate B. Lower extremity blood flow
and responses to occlusion ischemia differ in exercise-trained and
sedentary tetraplegic persons. Arch Phys Med Rehabil 1996; 77:
1260–1265.
5 Kocina P. Body composition of spinal cord injured adults. Sports
Med 1997; 23: 48–60.
6 Cruse JM, Lewis RE, Dilioglou S, Roe DL, Wallace WF, Chen RS.
Review of immune function, healing of pressure ulcers, and
nutritional status in patients with spinal cord injury. J Spinal Cord
Med 2000; 23: 129–135.
7 Marin PJ, Rhea MR. Effects of vibration training on
muscle strength: a meta-analysis. J Strength Cond Res 2010; 24:
548–556.
8 Hazell TJ, Jakobi JM, Kenno KA. The effects of whole-body
vibration on upper- and lower-body EMG during static
and dynamic contractions. Appl Physiol Nutr Metab 2007; 32:
1156–1163.
9 Kerschan-Schindl K, Grampp S, Henk C, Resch H, Preisinger E,
Fialka-Moser V et al. Whole-body vibration exercise leads
to alterations in muscle blood volume. Clin Physiol 2001; 21:
377–382.
10 Hazell TJ, Thomas GW, Deguire JR, Lemon PW. Vertical
whole-body vibration does not increase cardiovascular stress
to static semi-squat exercise. Eur J Appl Physiol 2008; 104:
903–908.
11 Lythgo N, Eser P, de Groot P, Galea M. Whole-body vibration
dosage alters leg blood flow. Clin Physiol Funct Imaging 2009; 29:
53–59.
12 Saltin B, Radegran G, Koskolou MD, Roach RC. Skeletal muscle
blood flow in humans and its regulation during exercise. Acta
Physiol Scand 1998; 162: 421–436.
13 Rittweger J, Ehrig J, Just K, Mutschelknauss M, Kirsch KA,
Felsenberg D. Oxygen uptake in whole-body vibration exercise:
influence of vibration frequency, amplitude, and external load.
Int J Sports Med 2002; 23: 428–432.
14 Davis R, Sanborn C, Nichols D, Bazett-Jones DM, Dugan EL. The
effects of whole body vibration on bone mineral density for a
person with a spinal cord injury: a case study. Adapt Phys Activ Q
2010; 27: 60–72.
15 Krassioukov A, Claydon VE. The clinical problems in cardiovas-
cular control following spinal cord injury: an overview. Prog Brain
Res 2006; 152: 223–229.
16 Ter Woerds W, De Groot PC, van Kuppevelt DH, Hopman MT.
Passive leg movements and passive cycling do not alter arterial
leg blood flow in subjects with spinal cord injury. Phys Ther 2006;
86: 636–645.
17 Bleeker MW, De Groot PC, Rongen GA, Rittweger J, Felsenberg D,
Smits P et al. Vascular adaptation to deconditioning and the effect
of an exercise countermeasure: results of the Berlin Bed Rest
study. J Appl Physiol 2005; 99: 1293–1300.
NP G _ S C _ SC 2 01 0151
Whole body vibration in spinal cord injury
AJ Herrero et al
5
Spinal Cord

UNCORRECTED PROOF
18 Torvinen S, Kannu P, Sievanen H, Jarvinen TA,
Pasanen M, Kontulainen S et al. Effect of a vibration
exposure on muscular performance and body balance. Rando-
mized cross-over study. Clin Physiol Funct Imaging 2002; 22:
145–152.
19 Cotey D, Hornby TG, Gordon KE, Schmit BD. Increases in muscle
activity produced by vibration of the thigh muscles during
locomotion in chronic human spinal cord injury. Exp Brain Res
2009; 196: 361–374.
20 De Cuyper H. The tonic vibration reflex]. Acta Belg Med Phys 1985;
8: 41–46.
21 Sherwood AM, McKay WB, Dimitrijevic MR. Motor control after
spinal cord injury: assessment using surface EMG. Muscle Nerve
1996; 19: 966–979.
NP G _ S C _ SC 2 01 0151
Whole body vibration in spinal cord injury
AJ Herrero et al
6
Spinal Cord