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Open Journal of Molecular and Integrative Physiology, 2013, 3, 158-165 OJMIP
http://dx.doi.org/10.4236/ojmip.2013.34021 Published Online November 2013 (http://www.scirp.org/journal/ojmip/)
Assessment of voluntary rhythmic muscle
contraction-induced exercising blood flow variability
measured by Doppler ultrasound
Takuya Osada1,2*, Bengt Saltin2, Göran Rådegran2,3,4
1Department of Sports Medicine for Health Promotion, Tokyo Medical University, Tokyo, Japan
2The Copenhagen Muscle Research Centre, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
3The Clinic for Heart Failure and Valvular Disease, Skåne University Hospital, Lund, Sweden
4Department of Cardiology, Clinical Sciences, Lund University, Lund, Sweden
Email: *DENTACMAC@aol.com
Received 25 September 2013; revised 25 October 2013; accepted 2 November 2013
Copyright © 2013 Takuya Osada et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
ABSTRACT
Given recent technological developments, ultrasound
Doppler can provide valuable measurements of blood
velocity/flow in the conduit artery with high temporal
resolution. In human-applied science such as exercise
physiology, hemodynamic measurements in the con-
duit artery is commonly performed by blood flow
feeding the exercising muscle, as the increase in oxy-
gen uptake (calculated as a product of arterial blood
flow to the exercising limb and the arterio-venous
oxygen difference) is directly proportional to the
work performed. The increased oxygen demand with
physical activity is met through a central mechanism,
an increase in cardiac output and blood pressure, as
well as a peripheral mechanism, an increase in vas-
cular conductance and oxygen extraction (a major
part of the whole exercising muscles) from the blood.
The increase in exercising muscle blood flow in rela-
tion to the target workload (quantitative response) may
be one indicator in circulatory adjustment for the ac-
tivity of muscle metabolism. Therefore, the determi-
nation of local blood flow dynamics (potential oxygen
supply) feeding repeated (rhythmic) muscle contrac-
tions can contribute to the understanding of the fac-
tors limiting work capacity including, for instance,
muscle metabolism, substance utilization and magni-
tude of vasodilatation in the exercising muscle. Using
non-invasive measures of pulsed Doppler ultrasound,
the validity of blood velocity/flow in the forearm or
lower limb conduit artery feeding to the muscle has
been previously demonstrated during rhythmic mus-
cle exercise. For the evaluation of exercising blood
flow, not only muscle contraction induced internal
physiological variability, or fluctuations in the mag-
nitude of blood velocity due to spontaneous muscle
contraction and relaxation induced changes in force
curve intensity, superimposed in cardiac beat-by-beat,
but also the alterations in the blood velocity (external
variability) due to a temporary sudden change in the
achieved workload, compared to the target workload,
should be considered. Furthermore, a small amount
of inconsistency in the voluntary muscle contraction
force at each kick seems to be unavoidable, and may
influence exercising muscle blood flow, although sub-
jects attempt to perform precisely similar repeated
voluntary muscle contractions at target workload
(muscle contraction force). This review presents the
methodological considerations for the variability of
exercising blood velocity/flow in the limb conduit ar-
tery during dynamic leg exercise assessed by pulsed
Doppler ultrasound in relation to data previously
reported in original research.
Keywords: Exercising Blood Flow; Doppler Ultrasound;
Muscle Contraction; Blood Flow Alterations
1. INTRODUCTION
In integrated and applied human physiology, blood flow
plays a key role, as oxygen transport via blood flow to
the working muscles is crucial for exercise capacity. Fur-
thermore, the magnitude of blood flow in the exercising
muscle may also be related to the blood volume redistri-
bution, via systemic circulation, as seen in previous
studies focused on cardiovascular regulation in humans
[1,2]. The oxygen uptake is evaluated by the product of
*Corresponding author.
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T. Osada et al. / Open Journal of Molecular and Integrative Physiology 3 (2013) 158-165 159
cardiac output and arterio-venous oxygen concentration
difference. Consequently peripheral conduit arterial
blood flow to the working muscle is one indicator of the
metabolic demand in local large muscle groups [3].
Moreover, detecting utilization in the leg requires com-
prehensive leg blood flow and arterio-venous substance
concentration difference [4,5].
Peripheral circulatory changes during exercise corre-
spond to the stress imposed on the cardiovascular system
[6,7]. Cardiac output increases with increasing exercise
intensity along with enhanced skeletal muscle vasodila-
tation and muscle pumping in the exercising muscle. As
the perfusion in the active muscle is one further indicator
of oxygen delivery to the muscles, blood velocity and
flow in the feeding conduit arteries to working skeletal
muscle may also give valuable information regarding the
hemodynamic response to exercise (particularly for large
muscle groups in the upper or lower limbs).
Recent advanced ultrasound Doppler instruments can
provide valuable measurements of arterial blood flow
with high temporal resolution in the cardiovascular sys-
tem. The determination of blood velocity in the feeding
conduit artery at rest and during rhythmic muscle con-
tractions during exercise has an impact on transient
changes in hemodynamics [6,8,9]. The investigation of
the blood flow supply due to continuous muscle contrac-
tions may require the evaluation of the effect of physical
activity on regulation among central and peripheral
hemodynamics.
Since one of the advantages of Doppler ultrasound is
that it can provide an evaluation of high temporal resolu-
tion blood velocity, the oscillation of blood velocity may
be detected at rest as a measure of heart beat and blood
pressure. During repeated muscle contractions of exer-
cise, these oscillations are even more pronounced, as
they are also influenced by intramuscular pressure varia-
tions. Therefore, the measurement of valid blood velocity
should be done carefully to account for the influence of
changes in the voluntary muscle contraction force in in-
ducing physiological blood velocity fluctuation (internal
variability), as well as the alterations in the blood veloc-
ity (external variability) due to a temporary sudden chan-
ge in the achieved workload compared to the target
workload.
Acknowledging the above mentioned variability in the
conduit arterial blood velocity, feeding into voluntary
rhythmic muscle contractions is valuable information for
the determination of exercising blood flow under various
muscle contraction intensities. The purpose of the present
review is therefore to summarize the physiological con-
siderations of the variability of the exercising blood ve-
locity/flow in the limb conduit artery during thigh mus-
cle kicking exercise (dynamic knee extensor exercise
model) assessed by Doppler ultrasound.
The paper is organized as follows: 1) Muscle contrac-
tion-induced physiological (internal) variations in blood
velocity during rhythmic muscle contractions, 2) Valida-
tion of exercising blood flow during rhythmic muscle
contractions and 3) Changes in exercising blood flow
(external variations) due to spontaneous changes of mus-
cle contraction force (workload) compared to target in-
tensity.
2. METHODOLOGICAL
CONSIDERATIONS
2.1. Exercise Model
Determinations of blood flow to contractile muscles are
the primary focus of the present review. Whole body
exercise methods such as walking and running on a
treadmill do not easily allow measurement of upper- and
lower-limb blood flow using Doppler ultrasound as mo-
tion artifacts are present. There is also difficulty in fixing
the ultrasound Doppler probe. Whole lower limb muscle
blood flow may be measured using the one-legged, re-
peated kicking (dynamic knee-extensor) exercise model
described by Andersen and Saltin [10]. In this exercise
model, the subject performs leg kicking while the leg is
passively returned by the cycle ergometer. Consequently,
the work is confined to the quadriceps muscle group and
the model allows stable measurements of femoral arterial
blood velocity using Doppler ultrasound because the
subject is seated (Figure 1). Therefore, all hemodynamic
data described in this review are from one-legged re-
peated kicking (dynamic knee-extensor) exercise with
the activation of the large thigh muscle group.
2.2. Hemodynamic Measurements
Ultrasound instrumentation: The measurements were
performed using a Doppler ultrasound instrument (Model
CFM 800, Vingmed Sound, Horten, Norway) equipped
with an annular phased array transducer (Vingmed
Sound) probe (11.5-mm diameter). The imaging fre-
quency was 7.5 MHz and the Doppler frequencies varied
between 4.0 and 6.0 MHz (high-pulsed repetition fre-
quency mode, 4 - 36 kHz). Blood velocity was measured
Figure 1. One-legged dynamic kicking (knee extensor) exer-
cise as a model of rhythmic thigh muscle contractions.
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T. Osada et al. / Open Journal of Molecular and Integrative Physiology 3 (2013) 158-165
160
with the probe at the lowest possible insonation angle
and always <60˚ [11]. The mean value of the insonation
angle was ~50˚, which remained constant throughout the
experiments for each individual. The probe position was
stable and the sample volume was precisely positioned in
the center of the vessel and adjusted to cover the diame-
ter width of the vessel.
Blood velocity, vessel diameter and blood flow: The
measurements of blood velocity and blood flow in the
femoral artery using Doppler ultrasound has previously
been validated and shown to produce accurate absolute
values both at rest and during leg exercise such as
rhythmical thigh muscle contractions [6,8,9,12,13]. Com-
pared with thermodilution, the high temporal resolution
of pulsed Doppler ultrasound additionally enables con-
tinuous measurement of blood velocity throughout the
knee-extensor exercise [6-9,14,15].
The angle-corrected, time and space-averaged, and
amplitude-weighted mean blood velocities were meas-
ured. Mean blood velocity was defined by averaging the
mean blood velocity trace, including both negative and
positive values [6,7]. The blood velocity parameter was
measured in relation to the blood pressure curve. The site
of blood velocity and vessel diameter measurements in
the femoral artery was distal to the inguinal ligament but
above the bifurcation into the branch of the superficial
and deep femoral artery. This location minimizes turbu-
lence from the femoral bifurcation and the influence of
blood flow from the inguinal region. In addition, the ar-
terial diameter is not affected by the contractions and
relaxations at this site, located proximal to the muscle.
The blood velocity measurements were performed
when steady-state had been reached after 3 min of one-
legged, dynamic knee extensor exercise, as previously
described [6,13,14]. The systolic and diastolic diameters
of the femoral artery were measured on a monitor rela-
tive to the electromyography at rest. The mean vessel
diameter was calculated in relation to the temporal dura-
tion of the blood pressure curve as; [(systolic vessel di-
ameter value × 1/3) + (diastolic vessel diameter value ×
2/3)] [6]. The diameters were measured under perpen-
dicular insonation at rest before exercise. The value of
the vessel diameter at rest (pre-exercise) was used to
calculate femoral arterial blood flow during rest and
during one-legged, dynamic knee extensor exercise,
since the diameter does not vary between rest and steady-
state exercise [1,6,12,16-18]. Steady-state one-legged
blood flow was calculated by multiplying the cross-sec-
tional area [Area = π × (vessel diameter/2)2] of the
femoral artery, with the angle corrected, time and space-
averaged, and amplitude (signal intensity) weighted
mean-blood velocity, where blood flow = mean-blood
velocity × cross-sectional area. Thus, the changes in
blood flow dynamics were basically parallel to the
changes in blood velocity.
Muscle force and work rate: Kicking muscle force
was measured using a strain gauge. Variations in muscle
force were taken to represent oscillations in intramuscu-
lar pressure, as these parameters have been shown to
temporally correlate closely to each other during dy-
namic knee extensor exercise [6,14,19]. The external
workload (work rate) was calculated according to the
knee extensor ergometer model [10,20], defined as: ex-
ternal workload (watt) = [contraction frequency (contrac-
tion per minute, cpm)/60 s] × [distance of one knee ex-
tensor revolution (6 m)] × [load (kg) × 9.81 (m/s2)]. The
specific loads applied were 0.333, 0.667, 1.0 and 1.333
kg at 10, 20, 30 and 40 watt, respectively, at 30 cpm; and
0.167, 0.333, 0.5 and 0.667 kg at 10, 20, 30 and 40 watt
at 60 cpm.
The external workload was evaluated by integrating
delta dP during the muscle contraction phase, where dP
(to time integral) = dF[N]i × R × Sin[alpha]i × revolution
per minute/60, were determined for each knee extensor
kicking session. The external workload = integral of dP
from time integral = 0 (where alpha = 0) to time integral
= x (where alpha = pi); dF[N]i, force (in Newtons) on the
kicking arm transducer to time integral; R, Length of
pedal arm in meters; Sin[alpha]i, Sin to horizontal angle
to time integral; revolution per minute, actual angular
velocity in rounds per minute to time integral; and
“dF[N]i × R × Sin[alpha]i” is the delta torque [Nm] to
time integral. The achieved workload determined by this
method was displayed in real time on a monitor visible to
the subjects, to maintain the target workload during dy-
namic knee extensor exercise.
3. EVALUATION OF EXERCISING
MUSCLE BLOOD FLOW
3.1. Muscle Contraction-Induced Physiological
Variations in Blood Velocity during
Rhythmic Muscle Contractions
Continuous recordings can clearly determine the magni-
tude of the physiological variability in blood velocity by
the contraction-relaxation-induced variations in muscle
force, and consequently the intramuscular pressure varia-
tions, along with the superimposed influence of the blood
pressure, as well as the tonic influence of the state of
vasodilatation [6,13,21]. The high intramuscular pressure
during muscle contractions may consequently temporar-
ily reduce or even reverse the blood velocity, depending
on the relationship between the intramuscular- and arte-
rial blood pressure. The major extent of the blood veloc-
ity and flow consequently occurs during the muscle re-
laxation phase [6,13,22]. Blood velocity fluctuated in
relation to the state of vasodilatation and the muscle con-
traction-relaxation duty cycles, indicated by the oscilla-
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T. Osada et al. / Open Journal of Molecular and Integrative Physiology 3 (2013) 158-165 161
tions in muscle force.
In general, the blood velocity increased to its highest
value at the systolic blood pressure phase during muscle
relaxation, and significantly decreased to its lowest value
at the diastolic blood pressure phase during muscle con-
traction (Figure 2). The blood velocity showed an inter-
mediate value at the systolic blood pressure phase during
muscle contraction and at the diastolic blood pressure
phase during muscle relaxation, respectively. The blood
velocity curve was furthermore retrograde in the diastolic
blood pressure phase during muscle contraction.
In Figure 3, the limited view of blood velocity profile
in relation to single muscle contraction-relaxation and
single cardio systolic-diastolic beat, as well as the blood
velocities during the systolic and diastolic phases were
found continuously in parallel with the blood pressure
curve during the muscle contraction and muscle relaxa-
tion phases determined from the electromyography and
the muscle force curve.
Four variations in the coupling between the blood
Time (sec)
Figure 2. Continuous recording of blood velocity in the
femoral artery, blood pressure and thigh muscle force during
steady-state one-legged dynamic kicking (knee extensor) ex-
ercise at 20 watts and 60 contractions per minute. The letters
depicted indicate; A: Muscle contraction at systolic blood
pressure phase, B: Muscle contraction at diastolic blood pres-
sure phase, C: Muscle relaxation at systolic blood pressure
phase, D: Muscle relaxation at diastolic blood pressure phase.
During rhythmic exercise, the peak thigh muscle force was
seen over or under target work load. The higher or lower
achieved muscle force (workload) may influence blood flow
values in Figures 5 and 6. Figure adapted from Osada and
Rådegran [21], reproduced with permission from Edizioni
Minerva Medica.
Time (sec)
Figure 3. Blood velocity profile for the systolic and diastolic
phases during the muscle contraction and muscle relaxation
phases at 20 watts and 60 contractions per minute. The arrows
down and up indicate the influence of the blood velocity, de-
pending on the magnitude of, and temporal relation between,
the muscle force (≈intramuscular pressure), the electromyog-
raphy (EMG) and the blood pressure, respectively. These pan-
els (A-D) are expanded by the part of blood velocity profile
corresponding to them in Figure 2. Figure adapted from Osada
and Rådegran [22], reproduced with permission from The
Physiological Society of Japan.
pressure curve and the state of muscle contraction and
relaxation were indicated; the systolic phase during mus-
cle contraction, the diastolic phase during muscle con-
traction, the systolic phase during muscle relaxation, and
the diastolic phase during muscle relaxation. The forma-
tion of the blood velocity profile and flow was influ-
enced by the intramuscular pressure, as indicated by the
muscle force curve, and the superimposed influence of
blood pressure in relation to the systolic and diastolic
phases. The magnitude of blood flow value measured
against the 4 variations indicates the large difference in
work rates during the muscle relaxation phase and those
of the muscle contraction phase at systolic and diastolic
points, respectively.
3.2. Validation of Exercising Blood Flow during
Rhythmic Muscle Contractions
In previous reports, peripheral hemodynamic measure-
ments have been performed using the thermodilution
technique for leg blood flow during dynamic knee-ex-
tensor exercise [10]. However, this invasive technique
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T. Osada et al. / Open Journal of Molecular and Integrative Physiology 3 (2013) 158-165
162
has the limitation of poor time resolution of blood flow.
Several other techniques have previously been developed
that enable estimates to be made of arterial inflow, ve-
nous outflow, and local blood flow within a muscle
[23-29]. Whereas many of the techniques are impaired
by different methodological limitations, the indicator
thermodilution and the ultrasound Doppler method have
both been found to give repeatable measurements of the
same magnitude during both rest and dynamic knee ex-
tensor exercise [6,30] (Figure 4).
Figure 4. Relationship between net-femoral arterial blood
flow (FBF) and target workload during dynamic knee
extensor exercise. The relationship between FBF and target
workload was positive and linear at 30 cpm (r = 0.997, P <
0.01, n = 4) and 60 cpm (r = 0.999, P < 0.05, n = 3), res-
pectively. The value of FBF for one subject was the average
value of 60 samplings at each session. Furthermore, the
target workload value in each individual subject was deter-
mined by averaging values of 60 samplings of the achieved
workloads at each session. Both FBF and target workload
were obtained from average values of all 9 subjects. Re-
gression equations are indicated as follows: FBF (l/min) =
1.71 + 0.083 × target workload at 30 cpm (solid line): FBF
(l/min) = 1.52 + 0.098 × target workload at 60 cpm (short
dotted line). These data are in close agreement with the
findings of Rådegran [6]: FBF (l/min) = 1.317 + 0.084 ×
target workload at 60 cpm, long dotted line. The difference
in absolute FBF was approximately 0.5 l/min between the
present FBF data and previous reports at 60 cpm by
Rådegran [6]. This difference may be due to the subjects’
characteristics, such as muscle strength variations and that
they worked at different percentages of the maximum volun-
tary knee contraction force. However, the slope of the re-
gression line in the present study is similar to previous
findings. cpm, contractions per minute. Data are expressed
as means standard error. Figure adapted from Osada and
Rådegran [32], reproduced with permission from John
Wiley & Sons Ltd.
There is a positive linear relationship between leg
blood flow in femoral artery and target work rate (10, 20,
30 and 40 watts) in relation to rhythmic thigh muscle
contractions at 30 and 60 contractions per minute (Fig-
ure 4). With the rapid increase in energy requirements
during exercise, equally rapid circulatory adjustments are
essential in order to meet the increased need for oxygen
and nutrients by the exercising muscle. In addition,
thermodilution blood flow measurements obtained under
similar experimental conditions by Andersen and Saltin
[10] are closely related to those obtained by Doppler
ultrasound. Thus, blood flow measured by Doppler ul-
trasound is valid not only at rest but also during incre-
mental one-legged dynamic knee extensor exercise.
The Doppler technique can be used to differentiate
between physiological and methodological variations in
flow, as well as detect rapid changes in flow induced by
exercise (dynamic or static), different metabolic states
(muscle contraction intensity or frequency), or any other
type of vasodilatation such as the reperfusion period after
arterial occlusion or infusion of a vasodilator substance.
3.3. Changes in Blood Flow Due to Spontaneous
Changes of Workload
Femoral arterial blood flow during steady-state rhythmic
thigh muscle contractions increases linearly with incre-
mental target workloads (work rates) [6,7,9,12,31]. This
implies that enhanced vasodilatation is elicited in relation
to the increased average muscle force, exerted at higher
workloads, to meet the elevated metabolic activity (Fig-
ure 4). However, these blood flow values are a mean of
steady-state exercising blood flow measurements, and
temporary muscle contraction-induced blood flow varia-
tions may therefore be conveyed in the mean average
blood flow value (Figure 5). For human voluntary exer-
cise, it is of value to consider how variations in repeated
muscle contractions at target muscle strength (muscle
force) directly influence exercise blood flow in conduit
arteries. Therefore, we have investigated whether sudden
physiological and spontaneous changes in exercise
rhythm, and consequently workload, temporarily alter
blood flow to the working muscle [32].
The results showed that femoral arterial blood flow
increased positively and linearly (dotted line) with in-
creasing target workload. However, femoral arterial
blood flow was inversely and linearly related (solid line)
to the actual achieved workload, when measured over 60
consecutive contraction-relaxation cycle bouts for each
target intensity at 30 and 60 contractions per minute,
respectively (see in Figure 5).
Thus any sudden spontaneous increase or decrease in
the achieved workload transiently altered the relationship
between limb femoral arterial blood flow and the
achieved workload. The influence upon the magnitude of
Copyright © 2013 SciRes. OPEN ACCESS
T. Osada et al. / Open Journal of Molecular and Integrative Physiology 3 (2013) 158-165
Copyright © 2013 SciRes.
163
limb femoral arterial blood flow, due to fluctuations in
the achieved workload from the target workload was
similar at target workload sessions of 30 and 60 contrac-
tions per minute, respectively. These findings indicate
that a transient sudden increase in the workload during
rhythmic muscle contractions more rapidly impedes
femoral arterial blood flow, and that vasodilatation may
be elicited to restore the intensity related steady-state
limb blood flow response, in relation to the average
metabolic activity (Figure 6).
This evidence may contribute to the evaluation of ex-
ercise hemodynamics for rhythmic, dynamic-isotonic
exercise training, leading to exercise prescriptions (mus-
cle contraction frequency or muscle contraction intensity)
for healthy participants, as well as for patients requiring
additional physical activity in a rehabilitation or clinical
setting.
Figure 5. Relationship between steady-state femoral arterial
blood flow (FBF) and the achieved workload during incre-
mental dynamic knee-extensor exercise at 30 or 60 contractions
per minute (cpm) during a minute measurement in one subject
(60 samplings at each workload). FBF was inversely related (P
< 0.05) to the actual achieved workload (60 samplings) at (A)
30 and (B) 60 cpm, respectively, for each target workload (solid
line). The linear relationship was furthermore positive (P <
0.0001) between FBF (240 samplings at 30 cpm; 180 sam-
plings at 60 cpm) and the target workloads (at 10, 20, 30 and 40
W at 30 cpm; and at 20, 30 and 40 W at 60 cpm) in one subject
(dotted line). Figure adapted from Osada and Rådegran [32],
reproduced with permission from John Wiley & Sons Ltd.
4. CONCLUSION
The detection of blood velocity with high temporal reso-
lution in real time, at rest, and during exercise, is the
advantage of using the non-invasive technique of the
Doppler method. However, the enhanced alterations in
Figure 6. Changes in femoral arterial blood flow (FBF) related to fluctuations in the achieved workload around the
target workload. A negative relationship was found between changes in FBF and changes in the achieved workload
from mean target workload at (A) 30 and (B) 60 contractions per minute (cpm), respectively. A higher achieved
workload, with a higher muscular force, reduced FBF. A lower achieved workload, with a lower muscular force,
increased FBF. The influence on the FBF magnitude due to fluctuations from the target workload was similar be-
tween the target workload sessions at 30 and 60 cpm, respectively. At both 30 and 60 cpm, changes in FBF were
within 0.6 and −0.6 l/min from baseline at the target workload in all sessions. Furthermore, changes in FBF ranged
between 0.2 and −0.2 l/min from baseline when the achieved workload was increased or decreased by ~2 W. The
target workload is defined as an average value (equal to mean workload) of 60 samplings for the achieved work-
load at each target workload (10, 20, 30, and 40 W). The basal FBF value at the mean target workload (diamond
shape) was measured as the average of the plotted FBF values between the mean target workload minus 0.5 W and
the mean target workload plus 0.5 W; which is defined by the horizontal standard (horizontal) line of the FBF
value (“zero”). Figure adapted from Osada and Rådegran [32], reproduced with permission from John Wiley &
Sons Ltd.
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T. Osada et al. / Open Journal of Molecular and Integrative Physiology 3 (2013) 158-165
164
blood velocity profile may potentially confuse the evalua-
tion of hemodynamics in the exercising muscles. This
review discussed muscle contraction-induced normal
physiological (internal) variations in blood velocity dur-
ing rhythmic muscle contractions, as well as changes in
exercising blood flow (external variations) due to spon-
taneous changes of muscle contraction force (workload)
compared to target intensity. These findings should be
considered when determining the precise physiological
net-blood velocity/flow values.
5. ACKNOWLEDGEMENTS
The staff of The Copenhagen Muscle Research Centre is greatly ac-
knowledged. The study was supported by the Danish National Research
Foundation Grant 504-14, Uehara Memorial Foundation in 2002, a
Grant-in-Aid for Young Scientists (B) in Scientific Research (No.
16700471) and the “Excellent Young Researchers Overseas Visit Pro-
gram” in Scientific Research (No. 21-8285) 2010 from MEXT and
JSPS.
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