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INTRAMUSCULAR BLOOD FLOW QUANTIFICATION WITH POWER
DOPPLER ULTRASONOGRAPHY
AMIR DORI, MD, PhD,1,2 HIBA ABBASI, BA,2 and CRAIG M. ZAIDMAN, MD2
1
Department of Neurology, Talpiot Medical Leadership Program, Chaim Sheba Medical Center, Tel HaShomer, and Joseph Sagol
Neuroscience Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel 52621
2
Department of Neurology, Washington University School of Medicine, St. Louis, Missouri, USA
Accepted 15 March 2016
ABSTRACT: Introduction: Quantification of blood flow to muscle
using ultrasound is limited to large vessels. Small vessel intra-
muscular blood flow cannot be quantified using ultrasound with-
out specialized methods or intravenous contrast. Methods: We
describe a technique using power Doppler to quantify postcon-
traction hyperemia in intramuscular vessels that can be used at
the bedside. Results: In 11 healthy subjects, postcontraction
intramuscular blood flow in the forearm flexors and tibialis ante-
rior muscles increased with stronger and repeated contractions.
Intravascular blood flow measured by pulsed Doppler in the
brachial artery similarly increased. Three patients with muscular
dystrophies showed a negligible increase of postcontraction
intramuscular blood flow. Conclusions: Intramuscular blood flow
can be quantified using power Doppler ultrasonography; it
increases following contraction and may be reduced in patients
with muscular dystrophies. This quantitative, noninvasive tech-
nique can be applied at the bedside and may facilitate studies
of disease impact on intramuscular blood flow.
Muscle Nerve 54: 872–878, 2016
Blood flow to muscle increases in response to
muscle activity. Seconds after a brief muscle con-
traction, intra-arterial blood flow rapidly increases
and peaks within 10–15 s.1–3 Quantification of
blood flow dynamics in response to muscle activity
typically is performed using pulse-wave Doppler
ultrasonography on a large artery supplying the
activated muscle, such as the brachial artery follow-
ing hand-grip contraction.3,4 This technique does
not assess blood flow in the smaller, intramuscular
vessels. Muscle disorders with pathology affecting
intramuscular vessels include myositis,5,6 Duchenne
muscular dystrophy (MD),7,8 and small fiber neu-
ropathy.9 Blood flow in these smaller, intramuscu-
lar vessels cannot be measured by pulsed Doppler
ultrasound and is, therefore, more challenging to
quantify than blood flow in larger arteries.
Power Doppler is sensitive for detecting slow
blood flow characteristic of small vessels and repre-
Additional supporting information may be found in the online version of
this article.
Abbreviations: MD, muscular dystrophy
Key words: blood flow; contraction; Doppler; dystrophy; muscle;
ultrasound
The study was supported by the Washington University in St. Louis Neu-
romuscular Research Fund, the National Institute of Health Neurological
Sciences Academic Development Award Grant Number K12 NS00169009
and the Institute of Clinical and Translational Sciences (UL1 TR000448).
Correspondence to: A. Dori; e-mail: amir.dori@sheba.health.gov.il
C 2016 Wiley Periodicals, Inc.
V
Published online 3 August 2016 in Wiley Online Library (wileyonlinelibrary.
com). DOI 10.1002/mus.25108
872 Muscle Blood Flow Sonography
sents the amount of blood present in the vascular
bed.10 The power Doppler signal is not directly
quantifiable at the bedside in commercially avail-
able ultrasound systems and is instead described
qualitatively.11–13 Prior techniques to quantify small
vessel intramuscular blood flow using power Dopp-
ler required either specialized techniques and cus-
tomized software,14 or intravenous contrast and
rigorously controlled protocols that are impractical
for use at the bedside.15
The goal of this study was to describe a nonin-
vasive method for quantifying intramuscular blood
flow that can be performed at the bedside in the
clinical setting using commercially available equip-
ment and a protocol suitable for both children
and adults. We used power Doppler ultrasonogra-
phy to quantify baseline intramuscular blood flow
and postcontraction hyperemia in the forearm
flexors and tibialis anterior muscles following dif-
ferent degrees of muscle activation. We also com-
pared power Doppler measures of intramuscular
blood flow in the forearm to pulsed Doppler meas-
ures of intra-arterial flow in the brachial artery and
compared healthy volunteers with patients with
MD.
METHODS
Subjects. The study was approved by the Washing-
ton University Institutional Review Board. All par-
ticipants gave written consent/assent. We enrolled
11 healthy control subjects (5 men/boys) consist-
ing of 8 adults (age 26–57 years; 4 men) and 3
children (ages 6, 8, and 10 years). All were right
hand dominant, denied histories of neuromuscular
or peripheral vascular symptoms, disorders involv-
ing the studied limbs, and diabetes mellitus. We
also enrolled 3 patients (men) with muscular dys-
trophies (Becker MD, ages 19 and 54 years; and
undefined limb girdle MD, age 54 years).
Exercise protocol. Subjects were examined lying
prone on an exam table in the supine position
with the arm supinated and feet extended just
beyond the edge of the examination table in a
neutral position to allow for unobstructed range of
motion at the ankle. Two subjects with MD pre-
ferred not to lie flat and were examined seated
with the arm slightly elevated and supported by a
MUSCLE & NERVE November 2016

pillow at the level of the heart. Subjects performed
single and repeated brief (1 s) muscle contrac-
tions. Single contractions were performed at vary-
ing degrees of effort as follows:
Forearm Flexors Assessment. Subjects were
instructed to quickly and briefly squeeze a hand-
held dynamometer (Jamar), to provide a minimal
(1/3 of maximal strength), moderate (2/3 of
maximal strength), or maximal effort, followed
each time by complete relaxation. Grip strength
(lbs-force) was recorded following each assessment.
Subjects were asked to estimate their force effort
(minimal, moderate, or maximal amounts), with-
out real-time feedback from the quantified grip
strength.
Tibialis Anterior Assessment. Assessment of the
tibialis anterior was performed only in healthy con-
trols. For obtaining minimal effort, subjects were
instructed to quickly and briefly dorsiflex the foot
against gravity. For obtaining maximal effort, sub-
jects were instructed to quickly and briefly dorsi-
flex the foot with maximal effort. Dynamometry
was not performed in the leg. At least 1 min of
rest was allowed between single contractions for
blood flow to return to baseline levels, which was
confirmed by imaging before each subsequent
exercise. For repeated maximal contraction, subjects
were instructed to perform repeated, brief (1 s)
maximal contraction (grip or ankle dorsiflexion)
immediately followed by 4 s of relaxation, for a
total of 2 min.
Ultrasonography Protocol. All ultrasound examina-
tions were performed using a Philips iu22 imaging
system with an L12–5 linear array probe. Two
investigators (A.D., C.M.Z.) obtained all ultrasound
images. We acquired axial ultrasound images of
the right forearm flexors and tibialis anterior
muscles at the junction of the proximal and mid-
dle thirds of the muscle. We held the ultrasound
probe perpendicular to the skin and used copious
transducer gel to ensure light transducer pressure.
Care was taken to ensure that probe positioning
was held constant throughout image acquisition.
All ultrasound system settings were held constant
for power Doppler assessment. Depth was set at 5
cm, power Doppler gain was set to 92%, and the
Doppler window was set to include the entire
image field. We recorded continuous cine video
loops. To capture results from single contractions,
we recorded for 30 s with 5 s of baseline at rest
before muscle activation, a brief (1 s) muscle con-
traction, and a postcontraction 24-s period. For
quantification of repeated maximal contraction
perfusion, we recorded a 2-min video with 5 s of
baseline at rest, followed by 1 min and 55 s of
Muscle Blood Flow Sonography
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repeated brief (1 s) contraction followed by 4 s of
rest.
Quantification of Intramuscular Blood Flow from
Power Doppler Images. We measured intramuscu-
lar blood flow using power Doppler, and we meas-
ured intra-arterial blood flow using continuous
pulse-wave color Doppler, as follows. Ultrasound
videos were exported and analyzed using ImageJ
(National Institutes of Health; Bethesda, MD). In
each video, we selected a region of interest that
included the entire visualized axial area of the
forearm flexors or tibialis anterior muscles, exclud-
ing skin and bone. We applied the same region of
interest to each frame in the video. There are 2
steps to quantify the power Doppler signal from
the ultrasound image: (1) selecting and (2) meas-
uring the amount of colored (power Doppler) pix-
els in the image. We selected only the colored
pixels (the power Doppler signal) and excluded
the gray-scale pixels (the soft tissue/bone back-
ground) using the thresholdcolour plugin (ImageJ)
with the following settings: color saturation, 80–
255, and brightness, 60–255 red/green/blue pix-
els. Once colored pixels were selected, we trans-
formed selected and unselected pixels to a binary
value (1-selected or 0-unselected). To quantify the
intramuscular blood flow, we measured the per-
centage area occupied by the selected (colored)
pixels within the region of interest in the muscle.
This procedure was applied to each frame within
the video, and results were exported to Microsoft
Excel.
Intramuscular Blood Flow Measures. We graphed
the intramuscular blood flow (% area within the
muscle occupied by blood flow) sequentially for
each frame of captured video. We identified fluctu-
ations of the intramuscular blood flow between sys-
tole and diastole and identified movement artifact
during contraction. We chose to only analyze
measurements during diastole. The baseline dia-
stolic intramuscular blood flow was calculated by
averaging the intramuscular blood flow during
diastole of 3–4 heart cycles at baseline. To measure
intramuscular blood flow after contraction, we
recorded the maximal diastolic intramuscular
blood flow following the contraction artifact. For
repeated contraction, we averaged a minimum of
10 diastolic intramuscular blood flow measure-
ments after maximal increase was obtained (asymp-
totic trend). We defined change in intramuscular
blood flow as the difference between the diastolic
intramuscular blood flow from baseline to after
contraction. We calculated the change in intramus-
cular blood flow in the forearm flexors and tibialis
anterior of each subject following the single and
repeated contractions.
MUSCLE & NERVE November 2016 873
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FIGURE 1. Grip contraction effort correlates with measured grip strength. (A) Measured grip strength increased with increased effort.
Grip strength of patients with muscular dystrophy was significantly lower than healthy controls but showed a similar correlation with
grip effort. (B) Power and pulsed Doppler measurements were obtained with similar grip strength. Control data are shown. Boxes
show the median line, lower to upper quartiles (25 to 75 percentile) and minimum to maximum extending lines. Outliers are marked by
a circle (extending 1.5 times the interquartile range) and squares (extending 3 times the interquartile range). Muscular dystrophy (MD),
minimum (Min), moderate (Mod), maximal (Max).

Intra-arterial Blood Flow Measures. We obtained
pulse-wave color Doppler recordings from the dis-
tal brachial artery in the right arm/antecubital
fossa using standard techniques.16 We placed the
sample volume window in the center of the artery
and obtained an insonation angle of 608 or less rel-
ative to the analyzed vessel. Similar to the protocol
for recording power Doppler images, we measured
intra-arterial blood flow using continuous pulse
wave Doppler at rest (5 s), and during and follow-
ing single minimal, moderate, and maximal muscle
contractions (additional 25 s). We measured the
total blood flow (cc/min) for each cardiac cycle
before (baseline) and after contraction. Similar to
the protocol for power Doppler, we calculated the
average baseline (average of 3–4 cardiac cycles)
and determined the maximal postcontraction
intra-arterial blood flow. Even small transducer
movement relative to the vessel during muscle con-
traction resulted in aberrant measures, and on sev-
eral occasions repeated attempts were required to
obtain technically satisfactory results. We could not
obtain intra-arterial blood flow during repeated
contractions due to movement. For each contrac-
tion performed, we waited at least 1 min between
repeated attempts to provide time for blood flow
to return to baseline. In 1 subject with MD, we
could not achieve a moderate degree of grip con-
traction during this assessment.
Statistics. We compared changes from baseline in
intramuscular and brachial artery blood flow
between different strength, single, and repeated
874 Muscle Blood Flow Sonography
contractions using repeated measures analysis of
variance with Bonferroni corrected group compari-
sons. We used t-tests or Mann-Whitney tests for
comparisons between independent groups. We
measured intra-rater reliability of intramuscular
blood flow from 4 control subjects who repeated a
single contraction of identical force. Statistical
analysis was performed using MedCalc for Win-
dows, version 14.12 (MedCalc Software, Ostend,
Belgium). Values are expressed as mean 6 stand-
ard error of the mean.
RESULTS
Grip Strength Measurements. Increasing grip effort
in controls showed a significant increase in muscle
strength (F 5 23.35; P < 0.001; Fig. 1A). Patients
with MD showed significantly lower moderate and
maximal strength (F 5 5.02; P 5 0.045). Grip
strength generated for power and color Doppler
measurements were similar (Fig. 1B; F 5 0.056;
P 5 0.814).
Healthy Controls. Intramuscular blood flow in
both the forearm flexors and tibialis anterior
muscles oscillated with the cardiac cycle (Figs. 2
and 3) and increased following contraction. At
baseline (rested muscle), intramuscular blood flow
was low (Fig. 2A,B,E,F), and at diastole was nearly
absent, with a mean of 1.20% 6 0.14 of the muscle
cross-sectional area in controls, and lower in MD
patients (0.17% 6 0.07; P < 0.001) . Movement of
the muscle during contraction resulted in an easily
identified movement artifact characterized by a
rapid and large increase in colored pixels lasting
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FIGURE 2. Power Doppler identifies intramuscular blood in cross sections of muscles. Power Doppler color signal in the forearm flex-
ors (A–D) and tibialis anterior (E–H) in diastole and systole in selected area of interest for quantification. The power Doppler signal in
yellow-red color shows increased intramuscular blood flow. An increase in the vascular flow (arrowheads) and additional vessels
(arrows) are detected following muscle contraction.

2–3 s (Fig. 3A,C). Following contraction, intramus-
cular blood flow increased (Fig. 2). This was evi-
dent by both an increase in blood flow in vessels
that were already identified at baseline and new
blood flow in vessels that were not identifiable at
rest (Fig. 2C,D,G,H).
Intramuscular blood flow increased in 2 phases
after a single contraction. There was an initial
Muscle Blood Flow Sonography
increase of intramuscular blood flow from baseline
immediately after resolution of the movement arti-
fact and a second additional increase in blood flow
that began 2–3 s later and reached a peak 13–16
s after maximal contraction of the forearm flexors
and tibialis anterior muscles, respectively (Supple-
mentary Fig. S1, which is available online). Blood
flow then gradually returned to baseline. In all
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FIGURE 3. Quantitative analysis of power Doppler signals. Intramuscular blood flow, measured as percent of muscle area occupied by
power Doppler signal, increases following contraction and is maximal following repeated contractions in both the forearm flexors (A,B)
and tibialis anterior (C,D). Oscillation of blood flow in muscle during the cardiac cycle is noted. Small arrows point to diastole at base-
line. During muscle contraction, a movement artifact is recorded as a large, rapid increase in signal. After resolution of the contraction
artifact, an immediate increase of blood in muscle is seen (phase 1), followed by a delayed, gradual, further increase of blood in mus-
cle (phase 2). A large arrow indicates the maximal diastolic intramuscular blood flow recorded for analysis. Repeated maximal contrac-
tion shows additional increase of blood within muscle which reaches a plateau within 40–60 s.

healthy subjects, intramuscular diastolic blood flow
reached a maximal (asymptotic) level by 60 s of
repeated contractions (Fig. 3B,D).
Intramuscular blood flow in both the forearm
and tibialis anterior increased with stronger and
repeated contractions (P < 0.001). In the forearm,
intramuscular blood flow was increased from base-
line by 1.73% 6 0.39 following minimal, by 2.85%
6 0.36 (P 5 0.2615) following moderate, and by
3.78% 6 0.35 (P 5 0.0013) following maximal grip
contraction. Intramuscular blood flow increased
most (7.26% 6 0.88; range 2.16–12.40%) following
repeated maximal grip contraction (P 5 0.0002;
Fig. 4A). Similarly, in the tibialis anterior (Fig.
4B), intramuscular blood flow increased (F 5
26.89; P < 0.001) with increasing contraction
strength. Intramuscular blood flow increased from
baseline by 1.61% 6 0.40 following minimal dorsi-
flexion effort, by 4.66% 6 0.80 following maximal
contraction (P 5 0.006), and increased most
(6.98% 6 1.05) following repeated maximal
effort contraction (P 5 0.0003). The intra-rater
876 Muscle Blood Flow Sonography
intra-class correlation coefficient for change in
intramuscular blood flow from baseline following a
single contraction was 0.96 for absolute agreement.
The increase in intramuscular blood flow fol-
lowing muscle contraction did not result solely
from increased venous return, as brachial artery
blood flow also increased with increasing grip
strength (F 5 9.96; P 5 0.001) (Fig. 5). The mean
blood flow in the brachial artery increased 157%
6 15 following minimal, 202% 6 19 (P 5 0.084)
following moderate, and 283% 6 33 following
maximal grip contraction (P 5 0.0113).
Muscular Dystrophy. Unlike controls, intramuscu-
lar blood flow in the forearms of subjects with MD
did not change (<1% difference from baseline)
following either minimal, moderate, maximal sin-
gle, or repeated maximal contraction (mean of
0.12, 0.14, 0.46, and 0.61% increase from baseline,
respectively; range following repeated maximal
grip contraction 0.39–0.78%) (Fig. 4). In contrast
to the intramuscular blood flow, the mean
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FIGURE 4. Postcontraction power and Doppler measurements. Intramuscular blood flow in the forearm flexors (A) and tibialis anterior
(B) increases with contraction strength. In 3 subjects with muscular dystrophy (dotted line), intramuscular blood flow did not increase
significantly following contraction. Muscular dystrophy (MD), minimum (Min), moderate (Mod), maximal (Max), repeated (Rep).

intra-arterial blood flow in the brachial artery often required to obtain technically accurate meas-
increased 120% 6 15 following minimal, 135% 6 urements of intra-arterial flow without probe repo-
3 following moderate, and 189% 6 30 following sitioning following contraction. This did not occur
maximal grip contraction. Following maximal con- during intramuscular power Doppler imaging,
traction, the percentage increase in intra-arterial which is less sensitive to angulation and more sen-
blood flow in the MD subjects was similar to the sitive to blood flow than pulse wave Doppler.19
healthy controls (Mann-Whitney test P 5 0.076). Quantification of the intramuscular blood flow
using power Doppler had high intra-rater reliability
DISCUSSION
in healthy muscle. Additional studies are required
We report a noninvasive method to quantify
to determine the inter-rater reliability in healthy
intramuscular blood flow from power Doppler
and diseased muscle. A trade-off of our technique
ultrasonography. This protocol can be applied at is that, unlike pulse wave Doppler or quantified
the bedside in both children and adults and does power Doppler following intravenous contrast,20
not require custom software. Similar to a prior we were not able to calculate actual blood flow or
study,14 we first quantified intramuscular blood volume quantities. Our intramuscular blood flow
flow by calculating the percent of muscle cross sec- measurements are relative values (% area), and
tional area occupied by the power Doppler signal the response to exercise is based on comparison to
and then measured changes in intramuscular baseline.
blood flow from baseline following muscle contrac- Blood flow to and within the muscle varies with
tion. Intramuscular blood flow was very low at rest effort. To control for this, prior studies of blood
and increased following a single brief contraction. flow response to exercise have used continuous
The immediate and delayed increase in intramus-
cular blood flow corresponds to the previously
described phase 1 and phase 2 of postcontraction
hyperemia.17 We also detected increased intramus-
cular blood flow with greater contraction strength.
These findings are consistent with prior descrip-
tions of blood flow response to exercise15,18 and
validate our methodology. In controls, both the
intramuscular and intra-arterial blood flow
increased with increasing muscle contraction. This
suggests that, although power Doppler does not
distinguish arterial from venous flow, the increase
in intramuscular blood flow we identified was not
from increased venous return alone.
Intramuscular power Doppler images were tech-
nically easier to obtain in both children and adults
than intra-arterial pulse Doppler flow measure-
ments. This is because minute movements in the FIGURE 5. Postcontraction pulse-wave Doppler measurements.
Intra-arterial flow in the brachial artery increases following grip
arm or transducer following muscle contraction contraction in healthy controls and in three subjects with mus-
compromised the optimal intra-arterial placement cular dystrophy. Muscular dystrophy (MD), minimum (Min),
of the Doppler tracing. Repeat assessments were moderate (Mod), maximal (Max).

Muscle Blood Flow Sonography MUSCLE & NERVE November 2016 877

grip dynamometry with real-time feedback to
achieve stringently controlled degrees of effort21,22
The equipment and subject training required for
this is unwieldy for use at the bedside and in young
children. We found that intramuscular blood flow
reached a maximal steady state following 60 s of
repeated maximal brief contractions. Therefore,
future studies could use a simpler protocol of base-
line assessment followed by 60 s of repeated, brief,
maximal contractions without continuous dyna-
mometry, immediately followed by quantification of
the intramuscular blood flow. Single or submaximal
contractions could also be studied but would
require controlled and measured effort.
This method for quantifying intramuscular
blood flow using power Doppler could be particu-
larly relevant for studying vascular dysfunction
related to neuromuscular disorders, such as dystro-
phinopathies21,23 and inflammatory myopathies6,12,13
as it may identify pathology that selectively affects
intramuscular vessels. The 3 subjects in our study
with MD showed an increase in blood flow in the
brachial artery similar to that seen in some normal
controls. But unlike the normal controls, they did
not show an increase in intramuscular blood flow.
Previous studies have also shown reduced intramus-
cular blood flow in patients with muscular dystro-
phies.7,8 In healthy controls, there is a variable
increase in intramuscular blood flow following
repeated exercise, which may possibly be affected
by fitness. Additional studies with more subjects are
needed to better characterize how muscle blood
flow differs in healthy controls as compared with
patients with MD and inflammatory myopathies. As
our technique is noninvasive and our protocol does
not require stringent quantification of strength, it
could facilitate investigations into how intramuscu-
lar blood flow changes in response to neuromuscu-
lar pathology.
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