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Power Doppler sonography: use in measuring alterations in muscle blood

volume after exercise

Article  in  American Journal of Roentgenology · July 1997

DOI: 10.2214/ajr.168.6.9168718 · Source: PubMed

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Joel Newman Ronald Adler

New England Baptist Hospital NYU Langone Medical Center
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 Power Doppler Sonography: Use in
Measuring Alterations in Muscle Blood
Volume After Exercise

Joel S. Newman1 OBJECTIVE. The purpose of this study was to show the ability of power Doppler sonog-
Ronald S. Adler raphy (PDS) to evaluate exercise-induced changes in muscle blood volume.
Jonathan M. Rubin SUBJECTS AND METHODS. We evaluated 20 biceps muscles with PDS in 10
healthy volunteers before and after they underwent a standardized exercise protocol. Intra-
muscular blood volume was qualitatively analyzed using a subjective scoring system to eval-
uate vascular conspicuity, comparing sonograms obtained before and after exercise. We also
collected preliminary data on the quantification of estimated fractional moving blood volume
(EFMBV) measured on sonograms obtained in eight biceps muscles of five volunteers. As-
sessment of significance was calculated using a Wilcoxon signed-rank correlation of signifi-
cance. The stability of relative changes in EFMBV was also assessed with measurements
performed at three different times in five healthy volunteers.
RESULTS. With exercise, all 20 biceps muscles showed a significant subjective increase in
apparent vascularity (p < .0005). Likewise, preliminaiy data on EFMBV showed significant in-
creases (p < .01) between baseline and peak exercise values (mean, 470%; range, 180-900%).
CONCLUSION. PDS revealed marked increases in intramuscular vascular conspicuity
after exercise. EFMBV provided a potentially useful parameter to document such increases
quantitatively.

T he
changes
evaluation
in
of exercise-induced
muscle is of ariportance
flow
tional
[6, 7]. Both
in nature,
techniques,
allow regional
being cross-sec-
estimates in
to exercise physiologists. sports blood flow.
physicians, and other individuals involved in Estimation of moving blood volume within
training performance athletes. Familiarity with muscle, as measured by power Doppler sonog-
normal and abnormal muscle physiology may raphy (PDS), offers an additional parameter in
also contribute to the evaluation of various mus- the evaluation of exercise-induced changes.
cle-disease states. Both metabolic changes and PDS is a relatively new technique that has been
altered blood flow occur within muscle during shown to significantly increase (by three to
exercise [1-5]. Currently, one of the most fre- five times) the sensitivity for depicting soft-
quently used techniques to measure the muscle tissue blood flow relative to conventional color
blood flow is venous occlusion plethysmogra- Doppler sonography [8] (Fig. 1). Applications
phy, which provides a global assessment of ex- have included improved depiction of renal
tremity blood flow [3]. No generally accepted microvasculature (i.e., cortical blush) and the
Received May 28, 1996; accepted after revision
imaging technique exists to assess regional alter- detection of hyperemia in musculoskeletal in-
November 15, 1996.
ations in blood flow. Such a technique would al- flammatory disease [9, 10]. A recently devel-
Supported in part by United States Army MRDC, BAA for
low evaluation of the response of individual o_ modification to the PDS technique
Breast Cancer Research, and Diasonics Corporation,
Milpitas, CA. muscle groups to a particular exercise protocol. allows quantification of relative moving blood
‘All authors: The Universityof Michigan Hospitals, or regional changes in blood flow in the pres- volume [1 1].
Departmentof Radiology - UHB1D5O2, 1500 E Medical Center ence of vascular compromise (i.e., peripheral In this preliminaiy investigation, we stud-
Dr., Ann Arbor, Ml 48109-0330.Address correspondence to
vascular disease). ied exercise-induced changes in moving blood
R. S. Adler.
Recent literature has shown that both MR volume using PDS to image the biceps mus-
AJR 1997;168:1525-1 530
imaging and conventional color Doppler imag- des of healthy volunteers. Our purpose was
0361-803X/97/1686-1 525 ing correlate well with other physiologic mea- twofold: to show, subjectively. that significant
© American Roentgen Ray Society sures of exercise-induced changes in blood increases in regional moving blood volume

AJR:168, June 1997 1525

 Newman et al.

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Fig. 1.-Comparison of mean-frequency and power Doppler maps after exercise in

healthy volunteer.
A, Transverse power Doppler sonogram ) P05 ) of biceps muscle obtained in healthy
male volunteer after three sets of 10 curls with 10-lb (4.55-kg ) weight ) pulse repeti-
tion frequency [PRF] = 1000 Hz and color gain = 111 dB).
B, Corresponding color Doppler sonogram using identical PRF and color gain as A
shows color noise distributed throughout image with total loss of vascular information.
C, Color Doppler sonogram with parameters identical to A and B (except with color
gain reduced to 102 dB to eliminate noise) shows improved flow sensitivity of PDS
approximately equal to 9 dB.

after exercise are well depicted using PDS; Subjects and Methods with no history of neuromuscular disease or
and to present preliminary data in which known injury to the biceps muscle or hicipital ten-
This study was completed in two stages. Ini-
quantification of fractional moving blood vol- don were evaluated. Both right and left biceps
tially. PDS of the biceps muscle before and after
muscles were examined using an identical proto-
ume within a region of interest (ROl) in the exercise was performed on both shoulders (ii = 20)
col. Eight volunteers were right hand dominant,
biceps muscle, after extensive exercise, pro- in 10 healthy volunteers. Qualitative analysis of
two were left hand dominant. Individuals chose 5-lb
duces a measurably significant alteration in flow patterns was performed. Subsequently. the
ability to quantify changes in fractional moving (2.27-kg) or 10-lb (4.55-kg) dumbbells (four and
the relative local moving blood volume be-
blood volume became available. Scans of exer- six volunteers, respectively ) on the basis of self-
tween resting and peak values.
cise-induced changes obtained in eight biceps assessment of strength.
We postulate, therefore, that PDS is sensi- All scans were obtained using a Spectra
muscles (five volunteers) were evaluated using
tive to exercise-induced changes in local in- (Diasonics, Milpitas, CA) and linear 10-MHz
the quantitative method described below.
tramuscular blood volume and therefore transducer. The proximal portion of the biceps
should be further investigated as a poten- Stage I muscle was scanned with the brachial artery and
tially useful adjunctive technique in muscle Twenty biceps muscles in 10 healthy volun- basilic vein used as landmarks along the medial
physiologic studies. teers ( 25-50 years old, four women and six men) image border. The skin was marked to assure that

1526 AJR:168, June 1997

 Power Doppler Sonography for Measuring Muscle Blood Volume

the same area was continually sampled. All scans Stage 2 Although changes in EFMBV were noted after
were performed at pulse repetition frequencies of each set, only the two well-defined endpoints-
Quantification of fractional moving blood vol-
1000 Hz with color gains of 1 1 1-1 1 2 dB. Identical ume depicted on PDS was initially described by Ru- baseline and peak EFMBV-were compared.
gain settings were used in scans obtained before bin et al. II II. Their analysis was performed with
Changes were computed as the relative value of
and after exercise. These parameters have been software developed in collaboration with the Dia-
EFMBV (rEFMBV), which is actually indepen-
empirically determined. using the Diasonics sonics Corporation. This software entails identifying dent of the green tag and instead reflects the rela-
equipment. as being adequate for most musculo- a vessel within a chosen ROl. A threshold knob is tive increase in power-per-pixel. A Wilcoxon
skeletal applications on the basis of our experience signed-rank correlation [121 was applied to the dif-
gradually adjusted, which appears as a green tag at
with more than 5(X) clinical cases in which PDS the highest PDS values. This threshold invariably
ferences between baseline and peak rEFMBV
has been performed. occurs within the included vessel, corresponding to (expressed as a ratio) to assign significance.
Baseline power Doppler scans were obtained of 100% blood. The threshold is selected to exclude the The stability of these measurements during a
both right and left sides before exercise. Scans vessel boundaries, in which partial volume effects given session and over time was examined as fol-
were obtained in transverse and sagittal planes. with the vessel wall will occur. This technique effec- lows: three EFMBV values were obtained before
The volunteer then performed three sequential sets tively produces a lowest upper bound (in PDS) with and after three sets of 10 curls with a fixed weight
of 10 curls ( 30 curls total ) using the dominant which to normalize the power-per-pixel within a in five volunteers (seven biceps muscles). each ac-
arm, after which scanning was repeated using the given soft-tissue ROl at approximately the same quisition representing a separate measurement in
identical protocol. The time between sets did not depth as the normalizing vessel. The ROl. in this which a new ROI was chosen to compute EFMBV.
exceed 30 sec. A preexercise scan of the opposite case, consists of an ellipse drawn within the color These acquisitions were then repeated for each vol-
side was then performed to evaluate changes in box from which the mean power-per-pixel is calcu- unteer at three different times (range. 8 hr to 18
blood volume related to any possible systemic ef- lated. In this manner soft-tissue attenuation and days). The same pulse-repetition frequencies. color-
feet of exercise and to obtain a new baseline. The transducer aperture effects are approximately elimi- gain settings and green-tag thresholds were main-
nondominant side was then scanned after a similar nated. Although this technique works well in vitro. tamed for each individual over time. A total of 21
exercise protocol. adjustments have been made to take into account po- data sets were available to assess mean EFMBV
All images were recorded on color laser print tential problems with the technique in its current variation for each session before and after exercise.
film ( Ektascan Medical Color Imager: Eastman form for in vivo applications. A total of seven data sets were available to assess
Kodak, Rochester, NY ). Scans were performed Preliminary data on quantification of exercise-in- mean rEFMBV over time.
and interpreted by two radiologists experienced duced changes were obtained from eight biceps mus-
with musculoskeletal sonography and PDS. Sub- des in five healthy volunteers (individuals scanned Results
jective evaluation of apparent vascularity was then more than once had these several weeks apart). One Stage I
performed. The following observations were re- volunteer ( scanned twice) was a conditioned weight
Among the initial 20 biceps muscles scanned,
corded for each case: the initial preexercise state. lifter who used a 44-lb (20-kg) dumbbell; the re-
apart from the brachial artety and vein, a few
changes in size of baseline vasculature. presence mainder were nonathletes. Three of the five volun-
(less than two to three) sparsely scattered yes-
of new vessels, and appearance of frank blush af- teers used 10-lb (4.55-kg) weights; one used an 8-lb
ter exercise. The resulting postexercise images (3.64-kg) weight. was first identi-
The brachial artery sels (‘2 mm in diameter) within the biceps mus-
were rank-ordered on the basis of observed fled on transverse imaging and “green tagged” for cle were generally evident at rest (Fig. 2). The
changes and a Wilcoxon signed-rank correlation the purposes of normalization; a mark was placed apparent vascularity score ranged from one to
applied to evaluate significance I I I]. over the arm at this location and the depth of the yes- four (mean, 1.8). After exercise, increased ap-
A subjective scoring system was established to sel used was documented. The brachial artery was parent va.scularity was evident in all 20 cases,
test significance using the following criteria. First. chosen for green tagging because arterial flow expe- with visualization of innumerable small intra-
the number of distinct visualized vessels in the riences less rouleaux formation, which could other- muscular vessels (mean score, 6.5; range, three
color box with diameter of 2 mm or greater were as- wise artificially reduce estimated fractional moving
toeight). A frank blush (blush score oftwo) was
signed a point value: one (five or fewer vessels). blood volume (EFMBV). The diminished rouleaux
present in 14 of 20 CaseS. After exercise of one
two (six-lO vessels), three ( I 1-15 vessels), four formation associated with arterial flow should also
arm. no significant subjective change was seen
( 16-20 vessels), and five (> 20 vessels). Second, result in a normalization that is more consistent
the blush score. defined by three or more vessels across subjects. on the contralateral preexercise scan. Left- and
with contiguous margins at some point. was as- A similar exercise protocol was employed for right-hand-dominant volunteers showed no
signed a value of zero (no contact). one (three or stage 2: a baseline EFMBV was obtained. fol- qualitative difference, with mean scores of 6.3
more vessels in contact but less than 50’k of the lowed by multiple sets of 10 curls each with power (range, five to eight) and 6.7 (range. three to
vessels within the portion of the color box overlap- Doppler scanning in the transverse plane. EFMBV eight). respectively. No significant subjective
ping the biceps muscle ). or two (greater than 50% was obtained immediately following each set. difference was found based on either the 5-lb
vessel contiguity in visualized biceps muscle for the Quantification consisted of placing an elliptical (2.27-kg) or 10-lb (4.55-kg) weights used, with
portion of biceps muscle in the color box ). Third. ROl within the portion of the biceps muscle in the
means of 6.1 (range, three to eight) and 6.8
the intramuscular vessel length was assigned a color box at approximately the same depth as the
(range. five to eight). respectively. The Wil-
score of zero ( no vessel exceeding I cm ). one (at normalizing vessel and calculating the EFMBV.
coxon signed-rank correlation II 11 applied to
least one vessel > I cm long. but none > 2 cm), or The ellipse excluded adjacent subcutaneous tis-
two (at least one vessel > 2 cm). sues. underlying bone. and brachial muscle. the the vascularity score difference obtained from
The sum of these values resulted in a compara- proximal end of which lies deep in relation to the pre- and postexercise scans showed significantly
tive score that could then be used for rank order- biceps muscle. All volunteers performed a mini- increased apparent vascularity (p < .0005).
ing. A negative result would consist of a mum of five sets of curls. Exercise was continued
Stage 2
postexercise scan in which apparent vascularity. until no further increase in EFMBV was evident or
based on these criteria, resulted in a lower numeri- the volunteer experienced significant fatigue ( i.e., Considerable variability was seen in base-
cal score than the corresponding preexercise scan. they could not complete an additional set of curls). line EFMBVs, which ranged from 1-16%

AJR:168, June 1997 1527

 Newman et al.

Fig. 2.-Power Doppler sonography

I (PDS) of biceps muscle in healthy

volunteer before and after exercise.
A, Transverse baseline PDS of left
biceps muscle. Note sparsely scat-
tered vessels within biceps muscle
as well as flow within axillary artery
and basilic vein ( arrows). Total vas-
cularity score = 1. Arrowheads =

humeral cortex.
B, Transverse PDS of left biceps
muscle after three consecutive
sets of 10 curls with 10-lb (4.55-kg)
dumbbell. Marked increase in ap-
parent vascularity within biceps
muscle is seen with increased
numbers of large and small intra-
muscular vessels. Total vascularity
score = 7.

( mean, 5.3% ), with the highest scores of 9% For practical reasons, multiple ROls could ercise and training 141: the onset of muscle
and 16% in the trained weight lifter (Fig. 3). not be evaluated between sets of curls using the fatigue associated with the accumulation of
When the same area was sampled after exer- current version of this software. In our experi- muscle lactate has been associated with
cise, a progressive rise in EFMBV was evi- ence, such measurements are stable within a states ofdirninished perfusion [ I, 5, 13, 15).
dent in all cases. Peak EFMBV was reached given image, so slight variations in ROl place- Flow imaging has become possible within
after a mean of 5.4 sets of curls ( range. three ment and size have little effect on the final re- the context of color (or power) Doppler im-
to eight sets). EFMBV then either plateaued sult. The areas employed within each ROI aging and MR imaging. Exercise-induced
(< I % variation ) or began to fall slightly. The consisted of a large number of independent changes in the gastrocnemius muscle have
rEFMBV with exercise was variable (mean, samples ( individual resolution elements ) over been shown to correlate well with color Dop-
4.7; range. 1.8 to nine). The trained weight which the EFMBV was calculated. A conser- pier imaging. Hirsch et al. )7J described an
lifter showed the highest baseline EFMBV vative estimate for the number of independent automated analysis system for extracting
( 16% ) but only a corresponding 1.8-fold in- samples from which the spatial averages were color Doppler information in which a veloc-
crease with exercise. Interestingly. albeit in performed to obtain the EFMBVs varied from ity segmentation algorithm had been applied
too small a population to draw any specific approximately 120 to 360 using a I -mm2 reso- to calculate the spatially averaged color
conclusions. such variability is in keeping lution element. In as much as the size ofthe res- Doppler signal. a parameter that closely re-
with other literature, as is the relatively small olution elements may be a factor of two smaller lates to soft-tissue perfusion. Likewise. exer-
increase in relative blood volume with train- than the value used, the actual number of inde- cisc-induced changes in local blood flow
ing 13. 4. 6). A signed rank test I 12) applied pendent samples contributing to the EFMBV have been documented on MR imaging and
to the differences in rEFMBV again was sig- estimates may be correspondingly larger. shown to relate to corresponding changes in
nificant (p < .01). the ankle-brachial ratio [61.
The stability of these measurements during a The ability to image and quantify local
Discussion
given session was then examined in five volun- changes in perfusion adds a new dimension to
teers ( seven biceps muscles ). The mean The response of normal skeletal muscle to evaluating exercise-related blood flow. The re-
EFMBV before exercise varied from 2. 1% to exercise has been the subject of many previ- sponse of individual muscle groups may be sep-
14.7%. with a mean SD of 1.1% throughout the ous investigations [1-6, 13-15], although arately quantified. as well as regional changes
2 1 sets of data. Likewise. the postexercise val- only on a limited basis within the imaging within a given muscle group. Flow heterogene-
ues ranged from 3.7% to 28.4%. with a mean literature [5, 6, 14]. Conventional physio- ity has been documented both temporally and
SD of 1.7%. The rEFMBV was the parameter logic evaluation of muscle blood flow in- spatially within individual muscle groups [31.
chosen to assess changes over time. The volves global estimates of perfusion vis-#{224}- Changes in local muscle blood flow and blood
rEFMBV ranged from I .5 to 2.5 with a mean vis venous occlusion plethysmography and volume may be seen with training and in is-
SD for the seven biceps muscles studied ( i.e., thermal dilution techniques in human sub- chemic states [1 , 4, 121. The differences in the
same biceps muscle studied at three different jects; regional estimates are possible using relative EFMBV between exercised gastrocne-
times) equal to 0.5. Similar results were ob- radiolabeled or colored microspheres [31. mius and soleus muscles in healthy volunteers
tamed if all 2 1 data sets were assessed individ- Radiolabeled and colored microspheres have and in a small group of patients with angio-
ually (i.e., not distinguishing one muscle from been employed in animal models of exer- graphically documented lower extremity periph-
another) as measurements occurring at differ- cise-induced changes. Changes in muscle era) vascular disease has been discussed
ent times with a mean rEFMBV of 1.9 (n = 21) blood flow. along with a host of metabolic (Gabriel H et al., American Institute of Ultra-
and an SD of 0.6. alterations, have been documented with ex- sound in Medicine meeting. March 1996).

1528 AJR:168, June 1997

 Power Doppler Sonography for Measuring Muscle Blood Volume

.- ---:

-- - -
--.-.

Fig. 3.-Determination of estimated fractional moving blood volume )EFMBV) with

exercise using power Doppler sonography (PDSI.
A, Transverse POS of biceps muscle before exercise. Ellipse delineates region of in-
terest (between plus marks in color box) from which EMFBV is calculated. Note
green-tagged brachial artery I arrow). Baseline EMFBV ( indicated by “blood volume”
in lower right corner) was 2.7%.
B, After 10 curls, EMFBV was 6.9%.
C, After a total of 30 curls, EFMBV was 12.4%. Based on conservative estimate for size
of resolution element, averages were computed with 260-400 independent samples.

PDS. which directly relates to the nutnber of cuity. although not surprising. also) indicates a from capillaries ( regardless of the manner in
scatterers producing a measurable Doppler fairly large dynamic range over which changes which the signal is acquired or displayed) and
shift. allows direct investigation of the moving in regional hkxxl flow within individual niuscle lack ofa true-time dependence. which would be
blood volume within soft tissue 7. 10J. Consid- groups may be qualitatively and potentially necessary for true pertl.ision to be calculated
erable improvement in dynaniic range is p()ssi- quantitatively assessed. Segmental muscle is- I I 1 j. Another problem with the method in its
ble relative to conventional color Doppler chetiia. for instance. could be apparent visually current fomi relates to choice of the correct nor-
sonography ( Fig. I ). The results are effectively and be qu;uitifiahle. The requirement for using malization. Rouleaux formation in blood flow
independent of velocity and flow direction. in exercise to exceed the limited vascular reserve results in increases in backscattered power and
contradistinction to conventional color Doppler in these patients to show the level of ischemia is so artificially reduces EFMBV. The higher
sonography. The limitations relate to lack of well known I I. 5. 131. shear rates associated with arterial flow should
Doppler sensitivity (e.g.. pulsed. color. or PDS has several potential clinical applica- result in less rouleaux formation and so provide
power) to detect capillary flow and the elimina- tiotis iii muscle disease. This technique may a better tionalization. serving as our rationale
tion of the effects of soft-tissue motion. represent an important adjunct in the identifica- for using the brachial artery rather than the vein.
EFMBV results from a spatial average over tioti of foci of ischemia-niyonecrosis. Al- Furthemiore. the nomialization ideally would
many independent saniples ( conservatively. though finditigs Ofl gray-scale sonography in be a continuous parameter. appropriately ad-
about l(X)-4(X). in the present case ) and is sta- compartment syndromes have been described justed for depth and aperture effects of the
tistically robust. I IS. 16). PDS niay prove useful in this regard. transducer. At this stage of development. the
In this study. PDS depicted marked apparent particularly in the dynamic evaluation of pa- normalization is. at best, an approximate correc-
increased vascular conspicuity within muscle tients with chronic compartment syndrome. tion for these effects. Radiologists must recog-
after exercise (p < .(XX)5). These qualitative Estimation ()f tractional tnoving blooxi vol- nize. however. that the relative change in these
changes were evident after a relatively short pe- ume with PDS has several potential limitations. values ( rEFMBV ) is unaffected by the choice
nod of exercise. The increased vascular conspi- including the inability to detect Doppler shift of normalization. These issues are expected to

AJR:168, June 1997 1529

 Newman et al.

be resolved with the development of algorithms gested to result in decreased requirements for pressures on responses to dynamic leg exercise in
to preselect the appropriate normalization and increased blood flow with exercise. Such an man. Eon App! P/oslo! 1988:57:772-776
6. Pena CS. McCauley TR. Price TB. Sumpio B, Gus-
derive correlation-based estimates of tissue alteration would be expected to produce in-
berg Ri, Gore JC. Quantitative blood flow measure-
transit time, as well as the use of sonographic creased basal blood volume levels in muscle,
ments with cine phase-contrast MR imaging of
contrast agents to markedly improve signal-to- with less substantial increase after exercise [4]. subjects at rest and after exercise to assess peripheral
noise ratios while eliminating the effects of mu- This phenomenon would be consistent with vascular disease. AiR 1996:167:153-157
leaux formation. observations in the trained weight lifter. 7. Hirsch W, Bell DS, Crawford DC, Kale SG, Mc-
Although only a small group of volunteers PDS appears to be a useful technique for Cready yR. Bamber JC. Colour Doppler imaging
analysis for tissue vascularity and perfusion: a
were studied quantitatively in this preliminaiy the depiction of changes in intramuscular
preliminary clinical evaluation. (Jltrasoiind Med
evaluation, all showed a substantial increase in moving blood volume after exercise. Further
Biol 1995:21:1107-1117
rEFMBV (p < .01). Our purpose herein was to refinements in the actual quantification of es- 8. Rubin JM. Bude RO, Carson PL, Bree RL, Adler
suggest a parameter that relates to altered blood timated moving blood volume may result in RS. Power Doppler: a potentially useful alterna-
volume after exercise. The relationship of blood the use of PDS as an additional tool for the tive to mean-frequency based color Doppler
volume to perfusion may not be entirely exercise physiologist. sonography. RadioIo,’v 1994: 190:853-856
9. Newman iS, Adler RS. Bude RO, Rubin JM. De-
stiaightforward because the laner quantity de-
Acknowledgments tection of soft tissue hyperemia: value of power
pends on both blood volume distribution and
Doppler sonography. AiR 1994; 163:385-389
capillaiy transit time. Iii fact, no a priori reason We thank Shelley McCarthy for her assis- 10. Bude RO. Rubin JM. Adler RS. Power vs conven-
exists to expect perfusion and blood volume to tance in the preparation of the manuscript tional color Doppler sonography: comparison in
be linearly related 131. One volunteer who was and Steve Spratt of the Diasonics Corpora- the depiction of normal intrarenal vasculature.
quantitatively studied on three occasions (at Radio!o,tv 1994: 192:777-780
tion, with whom the fractional blood volume
least 2 weeks apart) had baseline EFMBV mea- I I . Ruhin JM. Adler RS. Fowlkes JB. em al. Fractional
software was developed.
moving blood volume estimation using power
surements that varied by only 1%, and
Doppler imaging. Radiology 1995: I 97:183-190
rEFMBV values of 3.6-3.9.
I 2. Snedecor GW, Cochr.ui WG. Statistha! methods,
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1530 AJR:168, June 1997

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