studies on patterns and their ultrasonic dopplerdoppler technique for detection ofdirection ofmotion...

British Heart Journal, 1974, 36, 899-907.

Studies on arterial flow patterns - instantaneousvelocity spectrums and their phasic changes - withdirectional ultrasonic Doppler technique'

Yasuharu Nimura, Hirohide Matsuo, Tohru Hayashi, Akira Kitabatake, Shigeki Mochizuki,Hiroshi Sakakibara, Kanemasu Kato, and Hiroshi AbeFrom the First Department of Medicine, Osaka University Medical School; The Central Laboratory for Clin-ical Investigation, Osaka University Hospital; and The Institute of Scientific and Industrial Research, OsakaUniversity, Osaka, Japan

Flow velocity spectra of main arteries in 24 healthy adult subjects and 21 healthy aged subjects were trans-cutaneously studied using the directional ultrasonic Doppler technique.

I) The instantaneous flow velocity spectrum is continuous throughout a pulse cycle, and intensified nearthe instantaneous maximum velocity, especially in the earlypart ofa pulse cycle.

2) No reverse flow phase is observed in the common carotid artery except for a small momentary reversecomponent. A reverseflow phase is always exhibited in thefemoral artery and in many occasions in the othermain arteries; it follows the systolic forward flow phase. After the reverse flow phase the diastolic forwardflow phase appears. In some subjects a second reverseflow phase and thirdforwardflow phase are successivelyobserved.

3) The arterial bloodflow almost looks like a propagation ofa damped longitudinal oscillation.4) At the time of conversion between theforwardflow phase and the reverseflow phase, bothforward and

reverse components simultaneously coexist in a cross-section of the vessel.5) The arterialflow pattern is easily changeable in the arteries of the extremities, especially in the brachial

artery. Such an easy changeability is the essentialfeature of the arterial bloodflow.6) The propagation velocity of the flow velocity wave is more rapid in elderly subjects than in other adult

subjects. The reverse flow phase of the arterial flow pattern in the extrermties is more often observed inelderly subjects than in adult subjects. In the common carotid artery of elderly subjects the peak velocity isreduced so that the systolic rapidforward phase looks like a plateau.

Studies on the mode of flow in the blood vesselsshould give us much information on the conditionof the cardiovascular system. The ultrasonicDoppler technique offers a useful transcutaneousapproach to this study. The technique was originallyproposed by Satomura, Matsubara, and Yoshioka(1956) for the physical measurement of minor vibra-tions. It was also revealed that Doppler beatsoccurred from the blood flow in the blood vessels(Satomura, 1959; Satomura and Kaneko, I960).One of the present authors and others (Kato et al.,I962) showed that Doppler beats due to the blood

Received 26 November I973.

IThis study was supported in part by the Grant in Aid forDevelopmental Scientific Research of the Ministry of Japan.

flow were caused by the back scattering of the ultra-sound from the blood corpuscles in the flow. Thistechnique has been clinically applied to the bloodvessels by Kaneko and his associates (Kaneko et al.,I96I; Kaneko, Shiraishi, and Omizo, I968). Frank-lin, Schlegel, and Rushmer (i96i), Rushmer, Baker,and Stegall (I966), and Reid, Sigelman, and Nasser(1969) have also developed Doppler flowmeters.This technique has come to be widely used in theclinical field (Miyazaki, I965; Strandness, McCut-cheon, and Rushmer, I966; Strandness et al., I967;Benchimol et al., I968; Yao, Hobbs, and Irvine,1968; Evans and Cockett, I969; Balas, Segditsas,and Koutsopoulos, 1970; Benchimol, Barreto, andTeng Wei Tio, 1970; Joyner, Harrison, and Gruber,I971; Benchimol and Desser, 1972).

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goo Nimura, Matsuo, Hayashi, Kitabatake, Mochizuki, Sakakibara, Kato, and Abe

Satomura's Doppler technique could reveal theflow velocity; that is, the magnitude of velocity, butnot the direction. I.ecently, Kato and Izumi (I966,I967), Kato, Kakusho, and Izumi (I968), McLeod(I967), Light (I97I), Cross and Light (I97i), andPourcelot (197I) independently proposed theirmodifications of the Doppler technique for the de-tection of the direction of the blood flow as well as

the magnitude of velocity. A number of papers,by Strandness et al. (I969), Benchimol, Desser, andGartlan (1972), Kalmanson et al. (1972), Cross andLight (I97I), Light and Cross (I972), and so forth,have been published on the clinical application ofthe directional Doppler technique.A frequency discriminator, a zero-crossing

counter, and a sound spectrograph have been usedfor the display of the Doppler output from theblood flow (Kato, I966). Of the above-mentionedmethods, the sound spectrogram provides uniqueinformation concerning the blood flow, though itsuse is somewhat troublesome (Kaneko et al., I965,I970; Light, I970). In the present study an attemptwas made to examine the mode of the blood flow,i.e. the velocity spectrum of the blood flow and itsphasic changes, in the main arteries in healthy sub-jects with the frequency shift method proposed byKato et al. (I968) and Kato and Izumi (I966, I967),using a transcutaneous approach.

Subjects and methodsForty-five healthy subjects were examined: 24 of themranged from 22 to 38 years, ofwhom 2I were men and 3

were women; the 2I ranged from 6i to 83 years, ofwhom I0 were men and II were women. They were

shown to be free from cardiovascular disease by medicalhistory, physical examination, and the electrocardiogramat rest.The studies conducted on the subjects concerned the

characteristic features of the blood flow in the mainarteries with particular respect to any age differences.

I) Frequency shift method of ultrasonicDoppler technique for detection of directionof motionThe principle of the non-directional method of theDoppler technique is as follows (Satomura et al., I956;Satomura, 1957):

2V CosOfd= fo

Here v represents the velocity of a target, 0 is the anglebetween the direction of the motion and of the ultra-sonic beam, c is the sound velocity, fo is the frequency ofthe transmitter wave, and fd is the Doppler shift fre-quency. The Doppler shift frequency is proportionalto the velocity component of the target in the directionof the ultrasonic beam.

The Doppler technique was so modified that it mightdetect not only the magnitude of velocity of the target,but also the direction of velocity (Kato and Izumi,I966, I967; Kato et al., I968). In this case the reflectedwave of the frequency fo + fd was led to a detector with alocal oscillation of the frequency fo + fL, so that the fre-quency of the beat reads fL -fd

fL-fd=fL- Cfoc

If fL was properly set to be larger than Ifdl, the motiontowards the transducer, for which fd is positive, wasrepresented by a frequency lower then fL, and the motionaway from the transducer, for which fd is negative, wasrepresented by a frequency higher than fL. Thus, thismodification of the Doppler technique could detect thedirection of velocity ofthe target as well as the magnitudeof velocity.

2) Equipment and manipulationThe equipment used was constructed respectively byNippon Electric Co. and Hitachi Medico Co., the con-struction being supervised by Kato. The frequencyused was 5 MHz, and the frequency of the local oscilla-tion was 5 004 MHz or 5o005 MHz. The transducermade of barium titanate, 5 mm, 7 mm, or I0 mm in dia-meter, was divided into two parts, for transmission andreception, respectively.A sound spectrograph, made by Rion Co., was used

for the display of the Doppler output and a loud-speakerwas used as a monitor for listening to the Doppler out-put. In a spectrogram the level of fL was a tenative base-line for the display of the direction of motion (Fig. 2).The density of the write-out is related to the outputvoltage, which was proportional to the square root of thenumber of blood corpuscles per unit volume of the blood(Kato et al., I962).The examinees were placed in a supine position at

room temperature 20'-30°C. The examination wasbegun after a io-minute rest. The examiner confirmedthe pathway of the artery with his finger-tips; then theultrasonic beam was transmitted proximally along thevessel at an angle of 600 from the skin. If the vessel wasparallel with the skin, i KHz corresponds to 300 mm/sec of the velocity of the target.

After a little training, it was easy to distinguish thearterial Doppler beat from the venous one by monitoringwith the loud speaker. It was also easy to distinguish thetwo on the spectrogram.The common carotid artery was examined in the lower

half of the neck, the subclavian artery at the infraclavi-cular fossa, the brachial artery at the flexor side of theelbow joint, the radial artery just at the proximal regionof the wrist joint, the femoral artery in the inguinalregion, and the dorsalis pedis artery in the middle of theinstep.

ResultsThe features examined were the general configura-tion of the spectrographic pattern, the instant-aneous maximum velocity, the peak velocity, the



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Studies on arterial flow patterns 90I

Systolic forward flow phase)iastolic forward flow

Reverse flow

Forward flow

'Instantaneous maximum velocity

ECG

F I G. i The nomenclature used in the present study for the arterial bloodflow pattern. Systolicforward flow phase: time interval in which the flow velocity is high because of cardiac systole;first reverse flow phase: time interval after the systolicforwardflow phase and showing a distalto proximal flow; diastolic forward flow phase: time interval after the systolic forward flowphase or the first reverse flow phase and corresponding to cardiac diastole. The flow velocity islow in this phase; instantaneous maximum velocity: maximum velocity in a cross-section of thevessel in any instant in a pulse cycle; peak velocity: the highest velocity in a pulse cycle; de-veloped velocity: the highest velocity - end-diastolic flow velocity, i.e. velocity increment dueto cardiac systole; appearance time: time interval from the beginning of the QRS complex ofthe electrocardiogram to the beginning of the systolic forward flow phase; accelerationtime: time interval from the beginning of the systolic forward flow phase to the instant ofpeakvelocity.

appearance time, the acceleration time, and theacceleration itself (Fig. i).

I) Common carotid arteryThe typical configuration of the spectrographicpattern of the flow of the common carotid arterywas composed of the systolic forward flow phase,which corresponded to cardiac systole, and thediastolic slow forward flow phase, which corres-ponded to cardiac diastole (Kaneko et al., 1970)(Fig. 2). The systolic forward flow phase exhibitedtwo peaks. A small valley was noted between thesystolic forward flow phase and the diastolic for-ward flow phase, and this amounted to a smallmomentary reverse component in I3 subjects (Fig.2 and Table). The dicrotic notch on the carotidpulse tracing coincided with this valley. In somesubjects an irregular reverse component was

observed throughout the systolic and diastolicphases (Fig. 3). This phenomenon was left unex-plained and the question of whether it was due tovortex motion in the arterial flow or to a contam-ination of the Doppler output from the venous flowremains to be studied.The Doppler output seemed more intense on the

tracing near the instantaneous maximum velocity onthe spectrogram during the acceleration time andwas homogeneous in the whole frequency rangefrom zero to the instantaneous maximum velocityafter the peak of the systolic forward flow phase.This was also observed in all the other arteries ex-amined. The peak velocity in the common carotidartery was, in general, slower in the elderly. In thesystolic forward flow phase of the aged the first peakwas near the second peak in height so that they weregenerally plateau-like (Fig. 4).



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902 Nimura, Matsuo, Hayashi, Kitabatake, Mochizuki, Sakakibara, Kato, and Abe

TABLE Peak velocity, appearance time, acceleration, appearance of reverse flow phase and peak reversevelocity in each artery in adults and elderly. Here, acceleration is determined by dividing developed velocity byacceleration time

Reverse flow

No. Max. velocity Appearance time Acceleration No. Max. velocity(cm/sec) (sec) cm/sec2 (cm/sec)average (SD) average (SD) average (SD) average (SD)

Common carotid arteryadult subjects 23 II3-I (20-04) 0-II (ooi8) I438 (5I5.I) 4 9-5elderly subjects 2I 70-I (I752) O-II (OOI8) I044 (3015) 9 II-O (7-28)

P <o-oi NS P <o-oiBrachial artery

adult subjects 22 92-1 (I8-75) o-i8 (o-oi8) I072 (225-9) 8 I7-9 (4-79)elderly subjects 21 785 (17-07) o-i6 (0-022) 1077 (I86-2) I5 I4.3 (5-03)

o-oi <P <o-I P <o-oi NSRadial artery

adult subjects I5 75-3 (I6-99) 0-2I (0-0I3) 915 (203 5) 2 I3-3elderly subjects 2I 64-2 (i6-33) O-I7 (o0-OI7) II30 (255-8) 7 10-2 (2z25)

P <o-oi P<o-oi o-oi< P<o-IFemoral artery

adult subjects i8 88-2 (IO-52) 0-21 (O-OI9) 824 (I57-7) i8 3I-6 (6-8o)elderly subjects i8 ioIn8 (29-II) o-i6 (0-oI9) 1043 (288-2) i8 25-4 (9-56)

o-oi<P <o-i P<o-oi P<o-oi o-oi<P<oi

REVERSE8~

*S....-6sliW

FORWARD

FIG. 2 An example of the flow pattern of the com-mon carotid artery in a healthy subject. It is composedof the systolic and diastolic forward flow phases. Thesystolic forwardflow phase exhibits two peaks. A smallmomentary reverse component is noted between theabove-mentioned two phases (a 29-year-old man).

REVERSE ....

--t EGG -1KffztOc,mh.c

FORWARD 0s

FIG. 3 Another example of the flow pattern of thecommon carotid artery. It is left unexplained whetheran irregular reverse component throughout the systolicand diastolic forward flow phases is due to vortexmotion at a branching site or to a contamination of theDoppler output from the venous flow. This remains tobe studied (a 27-year-old man).

REVERSE

9, Ab. -,-B.S_|SIIin

I.. j CG _-2KHt(b0./,.0FORWARD o._s_v

FIG. 4 An example of the flow pattern of the com-mon carotid artery in the aged. In the systolic forwardflow phase peak velocity is so reduced that the heightof the first peak is almost the same as that of the secondpeak. The systolicforwardflow phase shows a plateau-like pattern (a 78-year-old woman).

Y IREVERSE

FORWARD

FIG. 5 An example of the flow pattern of thebrachial artery. In the systolic forward flow phase theheight of the second peak becomes so low that the flowpattern in this phase seems almost one-peaked; noreverse flow phase appears (a 29-year-old man).



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Studies on arterial flow patterns 903

2) Subclavian arteryThe pathway of the subclavian artery was not easilyidentified, making it difficult to get the desired anglebetween the ultrasonic beam and the vessel. Hence,there was noted a large distribution range of theresults obtained from examination of this artery.

REVERVE

u 9 ~~~~~~~~~~~~~-^21XHz1b0cm1m)s FORWARD-G 5 s

FIG. 6 Another example of the flow pattern of thebrachial artery. A reverse flow phase is observed fol-lowed by the diastolic forward flow phase. The bloodflow is stopped in the last stage of a pulse cycle (a 29-year-old man).

REVERSE

FORWARD '

REVERSE

w ECG _ H21.60cmhed

FIG. 7 Change of the flow pattern of the brachialartery due to a piece of ice put on the palm. a) Beforethe test; b) after the test: the flow velocity in thesystolic forwardflow phase is reduced, followed by thefirst reverse phase; the blood flow disappeared indiastole, except for the diastolic forward flow phaselasting only a short time (a 29-year-old man).

3) Brachial arteryIn the systolic forward flow phase of the brachialartery a peak corresponding to the second peak inthe common carotid artery was so low that the con-figuration looked single-peaked, and the duration ofthe main peak was shorter than the ejection time ofthe heart. Such a trend was commonly observed inall the main peripheral arteries mentioned in thisand the following sections (Fig. 5).

Various kinds of configurations in the flow patternof this artery were noted. In some subjects the bloodflow was unidirectional throughout a pulse cycle(Fig. 5). Other subjects exhibited the slow reverseflow phase after the systolic forward flow phase,followed again by the slower diastolic forward flowphase, and the blood flow almost stopped at the latestage of a pulse cycle (Fig. 6). In a third and inter-mediate pattern the blood flow almost stopped, butwas not reversed, between the systolic forward flowphase and the diastolic forward flow phase.The reverse flow phase was more often observed

in the elderly under physiologically stable conditionsat rest (Table).The blood flow pattern in the brachial artery

was readily changeable so that it easily shifted fromthe pattern without to the pattern with the reverseflow phase by an external cause, e.g. by putting apiece of ice on the palm (Fig. 7). Removal of thepiece ofice resulted in the return to the former bloodflow pattern. In some subjects the change was easilycaused even by being addressed by the examiner. Ingeneral, transition of the flow pattern from one kindto another quickly occurred within an interval ofseveral pulse cycles (Fig. 8).

4) Radial arteryThe peak velocity was slower in the radial arterythan in the brachial artery (Table).The flow pattern of the radial artery was not so

labile as that of the brachial artery (Table).

REVERSE

-W.W-.X1FORWARD 45s-c .:

2 Mt(60ciah cc)_

FIG. 8 Rapid change in the flow pattern of the brachial artery. When the examinee wasaddressed by the examiner, the flow pattern changed within an interval of several pulse cycles(a 25-year-old woman).



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5) Femoral arteryThe intensity of the Doppler output was muchhigher in the femoral artery than in the otherarteries in the extremities. In all the subjects ex-amined, the slow reverse flow phase occurred afterthe systolic forward flow phase (Table). Then, thereagain occurred the slower diastolic forward flowphase (Fig. 9). In some subjects, there were furtherobserved the second reverse flow phase followed bythe third forward flow phase, with a reduction in themagnitude of their velocity.

It was discovered that a forward flow componentand a reverse component coexist in the same cross-section of the artery at the time of conversion be-tween the forward flow phase and the reverse flowphase (Fig. 9). This was also noted in the otherarteries, but was most pronounced in the femoralartery.

6) Dorsalis pedis arteryThe intensity of the Doppler output was muchlower in the dorsalis pedis artery than in the otherarteries. In this artery, the flow velocity was usuallyslow. The reverse flow phase was observed in manycases.

REVERSE

FORWARD -2KH.fbO^/s.d

ECG------

FIG. 9 An example of theflow pattern of thefemoralartery. The reverse flow phase is noted after thesystolic forward flow phase. Then, there again occursthe diastolic forward flow phase (a 28-year-old man).

REVERSEDorscilispedisartery

Femorartery

1FORWARDECO

r (S~~~~~~~~~.5.>.e.t <-2Kz(K#/u

FIG. I0 Temporal relation between theflow patternsof the femoral artery and of the dorsalis pedis artery.The reverse flow phase is propagated from the proxi-mal to the distal artery after the preceding forwardflow phase (a 21-year-old man).

Propagation of the reverse flow phase was ex-amined in reference to the femoral artery and thedorsalis pedis artery. It was found that the reverseflow phase was propagated from proximal to distalafter the preceding forward flow phase (Fig. io).

DiscussionI) Velocity spectrum of blood flowThe instantaneous frequency spectrum of theDoppler output of the blood flow, i.e. the instant-aneous velocity spectrum, was continuous through-out a pulse cycle, as already shown by Kaneko et al.(i965, I970), Cross and Light (I97i), Light andCross (1972), and Light (1970). The velocity profileat a cross-section of a steady laminar flow of New-tonian fluid is known to be parabolic, so it wouldmake the velocity spectrum homogeneous from zeroto the maximum velocity at any instant. However,the instantaneous velocity spectrum of the arteryobtained in the present study was not necessarilyhomogeneous, but looked more intense near theinstantaneous maximum velocity especially duringthe acceleration time. This finding indicated that atthat time the blood flow is driven rather uniformlyin a whole section, i.e. with a flat velocity profile, sothat the blood flow would be considerably differentfrom that of the steady laminar flow of a Newtonianfluid.

2) Undulatory character of velocity pulse andpresence of reverse flow phasePeripheral arteries revealed, as a rule, an undula-tory flow even during the period corresponding todiastole of the heart; reverse components were alsooften exhibited. Such findings have already beenreported by Strandness et al. (I969) and Kanekoet al. (I970). The forward flow phase and thereverse flow phase repeatedly appeared one afterthe other, with the amplitude gradually reducing(Fig. 6). The reverse flow phase appeared moreoften in the middle part of the artery than in themore distal part, as shown in the cases ofthe brachialartery and the radial artery (Table). This seemed toresult mainly from the elasticity of the vessel wall ofthe middle part of the artery, in association withperipheral resistance, in terms of the Windkesseltheory. Interestingly enough, the duration of thesystolic forward flow phase in the peripheral arteriesproved to be much shorter than that of the cardiacejection period. Recently, Anliker and Rockwell(I971) theoretically studied the propagation of apressure wave in a tapered elastic tube with anassumption of one-dimensional motion of the in-compressible fluid. Their findings showed that asthe pulse wave is propagated, the wave front



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Studies on arterial flow patternts gos

steepens considerably with distance. The above-mentioned finding in the present study may corres-pond to those authors' theoretical consideration.

3) Propagation of velocity pulse waves andcoexistence of forward and reverse com-ponentsIn the arteries the reverse flow phase was propagatedfrom proximal to distal, following the precedingforward flow phase (Fig. io). This finding suggestedthat the reverse flow phase did not result from, 'arebound from the periphery,' but largely from thenature of the vessel wall, i.e. elasticity, as mentionedabove. The time sequence of flow velocity at a cer-tain site ofthe middle-sized artery was like a dampedoscillation (Fig. 6). Thus, the arterial flow can beregarded as propagation of the longitudinal wave ofsuch a damped oscillation from proximal to distalin the blood column, undergoing some modificationof the configuration and amplitude with distance.

It was revealed that the forward and reverse com-ponents transiently coexisted in a cross-section ofthe vessel at the time of conversion between for-ward and reverse (Fig. 9). Such a phenomenon wasalso noted by Strandness et al. (I969) who used thephase shift method of the Doppler technique. Pre-viously Womersley (I955) and Hale, McDonald,and Womersley (I955) studied the fluid dynamics ofa pulstile flow of viscous liquid in a solid tube.They theoretically showed that at the time of pulstilechange of the direction of flow the circumferentialflow changes its direction earlier than the centralflow, while the latter remains a forward direction,so that there transiently coexist the forward flowand the reverse flow in a cross-section of the tube.Sakamoto, Saito, and Nakayama (I966) performeda similar study using an elastic tube with a similarresult. The transient coexistence of the forwardflow and the reverse flow, revealed in the presentstudy, was assumed to correspond to the results ofthe above-mentioned theoretical consideration,though only the velocity spectrum was consideredin the present study, leaving velocity distributionundetermined.

4) Variability of flow pattern in arteriesThe blood flow pattern was easily changed even at adefinite site of the artery, being sensitive to andresponding to external conditions (Fig. 7). Kanekoet al. (I96I) previously reported that there is a closerelation between the blood flow pattern and roomtemperature. This variability was also reported byKobayashi (I97I). The response was immediate,occurring within several pulse periods (Fig. 8). Theeasy variability of the blood flow pattern is thus

assumed to be related to vasomotor activity. It hasbeen reported that lumbar sympathectomy resultedin an increase of effective flow and the disappearanceof reverse flow in the femoral artery (Lee, Castillo,and Madden, I970). Therefore, it is considered thatthe immediate appearance or augmentation of thereverse flow phase in the artery due to externalcauses is related to the increase of peripheral re-sistance due to vasoconstriction.This easy variability is considered to be one of the

essential features of the blood flow of peripheralarteries. It was obvious that the change was notrandom, but followed certain conditions.

5) Difference of blood flow pattern dependingupon ageThere was a notable difference in the arterial flowpattern with respect to age.The appearance time of the arterial flow pattern

was shorter in the aged than in adults (Mizuno,I969) (Table). Such a difference has been notedeven in a conventional pulse tracing. It had beeninterpreted as resulting from the acceleration of thepropagation velocity of pulse wave due to scleroticchanges of the blood vessels.

In the present study, the conditions of examina-tion seemed alike both for the elderly and the othersubjects. So, it was very significant that the reverseflow phase was more frequently detected in theelderly (Table). Considering the discussion in sec-tion (2) concerning the reverse flow phase, the fre-quent appearance of the reverse flow phase in theelderly was interpreted to suggest a higher peri-pheral resistance.Another remarkable difference was noted be-

tween the elderly and the other subjects in the flowof the common carotid artery. The flow pattern ofthis artery in the elderly seemed plateau-like in thesystolic forward flow phase (Fig. 4). Such a pheno-menon had been noted and interpreted as related tocerebral arteriosclerosis by Kaneko et al. (I970).Namely, in the elderly, the flow pattern of the com-mon carotid artery usually seemed less oscillatory,while those of the other arteries seemed moreoscillatory, as mentioned above (Hayashi et al.,197I). Such a difference between the commoncarotid artery and the arteries in the extremitiesmay be caused by differences in the distribution ofelasticity, resistance, and so forth, between thetwo arterial trees. Much remains to be studied aboutsuch problems in the future.

The authors wish to thank Dr. M. Miyazaki, KohsaiinHospital, for the referral of volunteers for this study.



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