Doppler Ultrasound in the Diagnosis of Peripheral Vascular Disease W. Robert Felix, Jr., M.D., Bernard Sigel, M.D., and George L. Popky, M.D.

I

N 1843 Christian Doppler describeda changein the perceived frequency of the energy wave emitted from a moving sound source.3This change in frequency is related to the velocity of the moving sourceand is known asthe Doppler effect. The most familiar example of this phenomenon is the change in pitch of a railroad train whistle as the train passesa stationary observer. When the approaching train blows its whistle, you hear a sound higher in frequency than the emitted sound-as the source races toward you compression produces more waves per unit time, and thus a higher frequency. As soon asthe train passesyou, there is an instantaneous decreasein the whistle sound frequency-the wavesare stretched out traveling back toward you. In 1959, Satormura21and in 1961 Franklin* describedinstruments that usedDopplershifted ultrasound signals to identify blood flow. Since then it has been used as a tool in evaluation of arteries,” to measureblood pressure,14P31r35 to diagnosevenousocclusion and incompetent valves, 25-27 and to study physiologic aspects of the cardiovascular system, such as arteria124*32and venousblood flow.6T22323 With the development of a pulsed Doppler ultrasound instrument by Baker in 1970,’ more precise determination of flow disturbancescan now be accomplished. The measurementof blood flow has also been achievedusing pulsed echo with Doppler instruments.” INSTRUMENTATION

Frequencies of 2.5, 5.0, 7.5, and 10 MHz have been used in the diagnosisof vasculardisease.The lower frequencies (2.5 MHz) tend to penetrate deeper and are used to examine slower moving structures, such as the fetal heart or arterial walls, W. Robert Felix, Jr., M.D.: Assistant Professor of Surgery, Harvard School of Medicine; Director, Vascular Diseases Laboratory, Veterans Administration Hospital, W. Roxbury, Mass. Bernard Sigel, M.D.: Dean and Bofessor of Surgery, Abraham Lincoln School of Medicine, Chicago, Ill. George L. Popky, M.D.: Professor of Radiology, Medical College of Pennsylvania, Philadelphia, Pa. 0 1975 by Grune & Stratton, Inc. Seminars

in Roentgenology,

Vol. X, No. 4 (October),

1975

while higher frequencies are used to detect blood flow in more superficial arteries and veins. All continuous wave Dopplers function in essentially the same manner. An ultrasound beam of known frequency is generated by a piezoelectric crystal and transmitted into tissue via a coupling gel. The sound wavesare reflected from the moving blood elements and reflected back to the skin. The frequency of these reflected wavesis altered from the initial frequency by an amount directly proportional to the velocity of the blood elements. The changein frequency of this Doppler shift is detected by the instrument, and the averagevelocity of the blood can then be calculated. The following equations describe the relationship between Doppler-shifted frequency, blood velocity, andincident angle: f = 2VfC @OS6) d

C

which upon rearrangementyields cfd u = 2f, (cos e)

where fd = Doppler frequency shift, f, = carrier frequency of instrument, c = velocity of sound in tissue (-1.5 X 10’ cm/set), v = velocity of blood cells, and 0 = angle between sound beam and velocity vector. If the transmitted carrier frequency is 5 X lo6 Hz and the angle is 60” (cos 8 = OS), then v = o.03fd cm/set. Under most clinical circumstances,the Doppler frequency shifts are within the audible range (500-5000 Hz), so that with appropriate amplification and a speakeror headphonesyou can “hear” blood flow. We have used three commercially available instruments* in our clinical studies and have found them all satisfactory. The directional Doppler16 presents frequency shifts representative of flow toward the probe in *Parks Models 805, 810 (nondirectional) and 806 (di-

rectional),Parks Electronics, Beaverton, Ore.; Medsonics Ultrasound Stethoscope, Medsonics Labs, Mountain View, Calif.; Doptone, Corbin-Farnsworth (SKI Co.) Palo Alto, Calif. 315

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one output channel and those of flow away from the probe in a second output channel. Phaseshifting is used to provide this impressionof directionality. Stereophonicheadphonescan alsobe usedto hear the flow “toward” in one ear and “away” in the other ear. An instrument reputed to be truly directional has been described recently.” The pulsed Doppler instruments can detect flow at a selected depth by turning the receiving amplifier on and off (gating) at the appropriate time.’ The instant of gating is set by a front panel control that can be calibrated. Currently available instruments can assessflow velocities in 1 mm incremental stepsacrossthe vesseldiameter. APPLICATIONS OF CONTINUOUS WAVE DOPPLER ULTRASOUND IN ARTERIAL DISEASE

The earliest and most frequent usesof Doppler ultrasound have been in the assessmentof the arterial system. Methods for monitoring of flow velocities before, during, and after vascular procedures,215110 in the diagnosis of peripheral and in measurement 15J1~32~35 carotid arterial diseases, of blood pressure,4*14and as a guide to the arteriographer12T28have been described. We shall discussonly the diagnostic applications and usesof Doppler ultrasound in planning arteriography. Absence of Flow

Approximately 2% of normal adults do not possessa superficial palmar arch, and 8% have inadequateflow. The presenceof a superficial palmar arch must thus be confirmed prior to cannulation of the radial artery for blood sampling or direct measurement of arterial blood pressure, since if the radial artery is injured during manipulation, the hand may not survive. One usually performs an Allen test for this purpose. This test is performed by having the patient make a fist while the examiner compresses both the radial and ulnar arteries. The hand is then opened, revealinga pale palm. The ulnar artery is releasedand the palm flushes if the superficial palmar arch is present and can function as a collateral vesselto the radial side of the hand. Whena patient is anesthetizedhe cannot cooperate to make a tight fist. If the need to carmulatethe radial artery arisesunder this circumstance, a Doppler instrument can be placed over the superficial palmar arch at the thenar eminence; then the compressionmaneuverscan be performed

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and the presence and patency of the collateral easily determined. Acute arterial embolism and spasmof arteries will both produce a pale and pulselessextremity. Whether this is spontaneous or results from cardiac catheterization or arteriography, the question is the same: Is it an embolus that demands immediate surgery, or is it a spasmthat will respond with time and vasodilators? If flow is detected by Doppler ultrasound in the distal (though pulseless)artery, the prognosisof the limb is favorable. Absence of flow has almost always been associatedwith fresh thrombus. We have found Doppler examination to be of value in determining the prognosis of a pulseless foot.’ Of 91 pulseless feet, 11% (10 limbs) required major amputation within 1 month. When Doppler flow was present, 5% (3 of 66) came to amputation. Whenthere wasno detectableDoppler flow in either of the pedal arteries, 20% of the limbs (5 of 25) required amputation within a month, in spite of attempts at salvageby vascular reconstruction in some cases. Gangrene and atrophy of the extremity’were the only other two significant risk factors. Ankle Blood Pressure and Pressure Index

Systolic blood pressure at the ankle can be readily measuredby locating Doppler flow at the dorsalis pedis or posterior tibial artery, inflating a pneumatic cuff on the calf to occlude the flow, and reducing the air pressureuntil flow is againdetected by the Doppler instrument. Measure of systolic pressure correlates with systolic pressure measurementobtained by the conventional method and with those obtained by using mercury-inrubber strain gaugeplethysmography.35The ultrasound method is less cumbersomethan plethysmography and more reliable than the auscultation method, which has a 10% failure rate in obtaining ankle pressures,evenin normal individuals. The ankle:brachial systolic pressure ratio or pressure index is normally always 1.0 or greater, ie, the arterial pressureat the ankle is equal to or slightly higher than the brachial artery pressure. In patients with symptomatic arterial disease,the pressure index is decreasedas the severity of symptoms increases.33Y3sThe pressureindex obtained in the resting state waslessthan 1.Oin 73% of limbs with arterial disease.More distal occlusions and multiple occlusionswere associatedwith

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Fig 1. Sound spectrograph of a normal femoral artery. Note the short-duration high frequency first sound followed by a lower frequency second sound and a return to baseline before the next first sound.

the lowest pressure indexes. Exercise produced a fall in the pressure index in all patients with arterial disease.This decreasewas likewise greater with multiple occlusions.g133 A longer time was required for the pressureindex to return to normal after exercise in patients with multiple lesions. After arterial surgery, it was noted that patients who had improvement in their pressure index (even though the foot may have remained pulseless)enjoyed a favorable prognosis. Diastolic aswell assystolic blood pressurecan be measured in the popliteal artery using a method describedby Kemmerer,14which detectswall motion. The measurementshave been shown to be more accurate than the standard auscultatory method in patients in shock and in infants.2g Using an automatedmethod for measuringsystolic and diastolic pressuresin the popliteal artery described by Poppers,” we have confirmed his findings. We also found that diastolic pressurechanges were in the same direction but of less magnitude than systolic pressurechanges.Diastolic pressure, therefore, adds no information to the evaluation of peripheral arterial disease. Diagnosis by Quality of Doppler Signals

Arteriovenous fistula is identified by noting an arterial signal over a subcutaneousmass3’ or by identifying a churning sound, presumably caused by the turbulent jets. We have been able to precisely locate the site of a brachial artery-cephalic vein fistula by this method in a situation where the arteriogram revealed only a massof dilated tortuous veins over the entire limb. Stenosisof the femoral artery hasbeen detected by noting an increase in the frequency of the Doppler-shifted signal as the transducer is passed along the vessel.30Becauseof the changein depth of the femoral artery asit passesinto the adductor canal and becauseof the difficulty of maintaining a constant transducer angle, we have not found this technique of mapping an artery to be useful. The diagnosis and approximate location of an

arterial lesion in the lower extremity can be determined by assessingthe quality of the sounds at four sites on the limb. The normal limb arterial flow sound (Fig 1) consists of a high frequency first sound of short duration followed by a lower frequency, longer second sound. Occasionally a third or fourth sound is heard. There is always a pause before the next high frequency first sound. Arterial abnormalities proximal to the monitoring site produce changesin these normal sounds, as presented m Table 1. The four sites (common femoral, popliteal, posterior tibial, dorsalis pedis) are monitored and the site of the lesion is estimated. The sensitivity of this method comparedto arteriogramswas 77% for 3 1 iliac lesions, 82% for 38 superficial femoral lesions,92% for 13 posterior tibial- lesions, and 100% for 13 anterior tibial lesions. The impressions gained from this examination have proved useful in a number of ways: (1) indicating whether arterial diseaseis the cause of a patient’s leg pain, (2) evaluatingthe pulselesslimb, (3) studying the contralateral asymptomatic limb to determine if it should be studied more extensively, (4) identifying patent distal vesselsto guide the arteriographer(seebelow), (5) monitoring during operations to establish the effect of endarterectomy or of bypass,(6) determining postoperative results, and (7) evaluatinglimbs with minimum Table 1. Diagnosis of Arterial Occlusion by Quality of Doppler Signals Quality

of Signal

1. High pitched first sound, lower pitched second sound, followed by a pause 2. Low pitched first sound, no second sound 3. Prolonged low frequency first sound, undulating, continuous 4. No Doppler signal

Interpretation Normal

Partial

occlusion

proximally

Complete occlusion proximally; flow is via collaterals Complete occhtsion proximally with no collaterals

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symptoms serially to identify progression of disease. The use of the Doppler as a guide for the arteriographer bears further comment. Doppler ultrasound instruments are excellent bubble detectors. A Doppler placed over an ankle artery identifies the passageof a bolus of contrast material (probably by detecting microbubbles). The ultrasound signal can thus be used to trigger the cassette changer so that films are taken as the contrast material reachesthe ankle.12Soulen reported casesin which the arteriogram indicated no runoff vessels,but becauseof Doppler ultrasound evidence of flow via collaterals to the foot the examination was repeated with films delayed as long as 48 set, and distal vesselssuitable for small vessel anastomosis became apparent, thus permitting a limb-savingoperation. Diagnosis of Carotid Artery Disease

The normal common carotid artery signals are similar to those of the femoral artery (ie, first sound and second sound) except that there is no pause(return to baseline) after the second sound. Instead, there is a continuous sound until the next first sound. Sound spectrogramsshow this diastolic flow.13 We have obtained similar sound spectrogramsin normal patients and after radical neck dissection (which rules out contributions by adjacent jugular veins). It is believed that the continuous flow pattern is due to the fact that the vessels supply a low resistancevascularbed. In partial occlusion, the continuous aspectof the carotid flow disappears.As diseaseprogresses,further changes similar to those described above for extremity artery occlusion are heard. This audible output is adequateto make somediagnoses. The Doppler ophthalmic artery test is useful for identifying occlusion and high gradestenosisof the internal carotid. r5 It is based on the observation that the direction of blood flow in the supraorbital artery (a terminal branch of the ophthalmic, which is the first intracranial branch of the internal carotid) is normally outward from the orbit and toward the forehead. When there is high grade stenosisor occlusion of the internal carotid artery, the flow in the supraorbital artery is reversed,and is toward the orbit. Collateralsfrom the superficial temporal and facial arteriessupply the supraorbital. The Doppler ophthalmic test is performed by locating the supraorbital artery with the Doppler

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instrument and noting the direction of the flow sound. Compression of the ipsilateral superficial temporal artery normally causesno change or a slight increase in the flow velocity. When there is occlusion or high grade stenosis of the internal carotid, however, compressionof this vesselcauses diminution or cessationof flow in the supraorbital artery. Diagnosis of Venous Disease

The absenceof spontaneousflow sounds at the femoral vein indicates the possibility of venousocclusion,30 but the use of augmentedflow soundsis more reliable.26 The diagnosisof venousocclusion is basedon the absenceof an augmented flow sound upon compression of the extremity distal to the monitoring site. Examination at the femoral vein is all that is necessaryto evaluate occlusion in the deep veins of the lower extremity. A spontaneousflow sound (S sound) is usually heard over the femoral vein. This sound is reminiscent of wind rushing through tree leavesand is cyclic with respiration. It is higher pitched (faster flow) on expiration. Compression of the thigh and the calf and dorsiflexion of the foot produce an augmented flow sound (distal positive A sound) if the deep venous system is patent. The diagnosis of incompetent valves is slightly more complex but is also basedupon augmented sounds. Incompetent valves are detected and located in one of two ways: (1) Production of an augmented sound upon compressionproximal to the monitoring site (as blood is forced retrograde through the incompetent valves). We call this a proximal positive A sound. (2) Production of an augmented sound upon release of compression distal to the monitoring site (as blood is allowed to flow retrograde past incompetent valvesto fill the veins emptied by compression).Wecall this a distal negative A sound. Figure 2 summarizesthe diagnosisof venousdisease. In a validative study, Doppler ultrasound examination was compared to clinical examination in 147 patients (248 extremities) in which the true status of the veins was determined by venogram, operation, or autopsy. The Doppler sensitivity in recognizingocclusion was 76%,while clinical sensitivity was only 54%.27There were 9% false positives. In new venographic occlusion (ie, no evidence of collateral channels) Doppler sensitivity

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CAUDAD

CanlALAD *-mLCTIcu

Fig 2. Schematic reprasention

of FLOW

of the diagnosis of venous occlusion and incompetent

became78% while clinical sensitivity improved to 66%.

The ultrasound technique is more sensitive in detecting occlusion of the larger thigh veins than in the smaller calf veins. Of 55 confirmed occlusions in the thigh, the ultrasound diagnosiswas correct in 46 (a sensitivity of 84%). Yao* reported a sensitivity of 93% (with 13% false positives) in Iliac vein thrombosis. Sincethe preciselocation of venouslesions is not always a prerequisite for institution of therapy, a clinical impression supported by ultrasound evidence of occlusion is adequateinformation upon which to base an intelligent therapeutic decision. Since ultrasound evidence of occlusion is so specific (only 9% false positives), it is probably enough evidence for recommendinganticoagulant therapy, evenwithout supportive clinical evidence. In a recent epidemiologic study,s5 the incidence of pulmonary embolism 1 week postoperatively in patients positive for ultrasound occlusion was 6 times that of the baseline group (clinically and ultrasound negative), and the incidence of pulmonary embolism in patients both clinically and ultrasound positive was 13 times that of the baseline group. The Doppler ultrasound technique is againmore sensitive than clinical examination for recognizing incompetent valves, but it gives more false positives. Thus the venous examination by Doppler

valves using Doppler ultrasound.

ultrasound is useful in evaluating the swollen leg, establishing the status of the deep veins prior to varicosesurgery, and predicting pulmonary embolism. It is the only noninvasive method for diagnosing incompetent valves. APPLICATIONS OF PULSED DOPPLER TECHNIQUES

Ultrasound Arteriography

By using a position sensingdevice attached to the pulsed Doppler transducer and by displaying the Doppler signalson the oscilloscope,Hokanson et al” “paint” a length of about 5 cm of carotid or femoral artery on the scope(Fig 3). The resolution does not approach that of a roentgen arteriogram but lateral and A-P views are easily obtained with no morbidity. Occasionally a lesion may be seen that was missed on the contrast arteriogram becauseof the densecontrast media. The ultrasound arteriogram is limited to a few centimeters of vesseland is therefore most useful in examining a high risk area such as the carotid bifurcation. Identification

of Disturbed Flow

Wehavebeen using pulsed Doppler ultrasound in our laboratory in an effort to identify disturbed flow states. We reason that small disturbancesof anatomy (plaques, stenosis, atheromatous ulcers)

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Fig 3. Normal carotid bifurcation as displayed by (A) pulsed Doppler ultrasound arteriogram and (B) contrast arteriogram. (Courtesy of Drs. D. S. Sumner, D. E. Strandness, Jr., D. E. Hokanson, and V. Bryan, University of Washington, Seattle.1

should produce flow disturbancesand thus an abnormal sound spectrogram pattern. We have observed that sound spectrogrampatterns from the central stream of normal arteries are devoid of low-frequency components in the midportion of the pulse display. The energy is concentrated in a narrow band, rising and falling asthe velocity pulse passes(Fig 4, bottom). Whena lesion causesa flow disturbance, the central-streamsound spectrogram has a more uniform distribution throughout the pulse contour (Fig 4, top). These abnormal patterns persist up to 15 cm distal to a lesion. Doppler techniques will probably not replace arteriography or venography, but currently available techniques can aid in performing angiographic studies more judiciously, and occasionally spare the patient an unnecessarystudy. The advantages

Fig 4. Internal carotid artery stenosis. Sound spectrogram (bottom) of the central stream pulsed Doppler signal at the common carotid is normal. Sound spectrogram (top) from the center of the stream at the internal carotid distal to the lesion is grossly abnormal (reduced frequency and presence of low frequency components throughout the entire spectral plot).

of the Doppler ultrasound technique are its safety, portability, economy, and reproducibility. As the state of the art progresses,we can expect more uses for Doppler ultrasound in the diagnosisand managementof vasculardiseases.

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pulse wave propagation velocity in hemorrhage. Arch Surg 102:53-56,197l 7. Felii WR Jr, Sigel B, Gunther L: The prognosis of the pulseless extremity as determined by Doppler ultrasound. Philadelphia Academy of Surgery, Dee 1973 8. Franklin DL, Schlegel W, Rushmer RF: Blood flow measured by Doppler frequency shift of back-scattered ultrasound. Science 134:564-565,196l 9. Fronek A, Johansen KH, Dilley RB, et al: Noninvasive physiologic tests in the diagnosis and characterization of peripheral arterial occlusive disease. Am J Surg 126:205-214,1973 10. Hardy DG, Eadie DGA: The use of ultrasound in the evaluation of peripheral vascular disease. Br J Clin Pratt 26~3-8, 1972

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11. Hokanson DE, Mozersky DJ, Sumner DS, et al: Ultrasonic arteriography : A noninvasive method of arterial visualization. Radiology 102:435-436, 1972 12. James PB, Galloway RW: The ultrasonic blood velocity detector as an aid to arteriography. Br J Radiology 44:743-746, 1971 13. Kaneko J, Shiraishi J, Omizo H, et al: Analysis of ultrasonic blood rheogram by the sound spectrograph. Jap Circ J 34:1035-1045, 1970 14. Kemmerer WT, Ware RW, Stegall HF, et al: Indirect measurement of human blood pressure by the Doppler ultrasound technique. Surg Forum 18:163-165,1967 15. Machleder HI, Barker WF: Stroke on the wrong side: Use of the Doppler ophthalmic test in cerebral vascular screening. Arch Surg 105:943-947, 1972 16. McLeod FD: A directional Doppler flowmeter. Digest of the Seventh Conference of Medical Biology. Stockholm, Engre, 1967 17. Nippa JH: Ultrasonic Doppler velocity meter for quantitative forward and reverse blood flow velocities. 19th Annual Conference Am lnst for Ultrasound in Med, Ott 1974, Seattle 18. Poppers PJ, Hochberg HM, Schmalzbach EL: A method for ultrasonic measurement of blood pressure in the adult leg. Anesthesiology 38:490-494, 1973 19. Reagan TR, Miller CW, Strandness DE Jr: Transcutaneous measurement of femoral artery flow. J Surg Res 11:477-482,1971 20. Rushmer RF, Baker DW, Stegall HF: Transcutaneous Doppler flow detection as a nondestructive technique. J Appl Physiol21:554-566,1966 21. Satormura S: Study of the flow patterns in peripheral arteries by ultrasonics. J Acoust Sot Japan 15:151153,1959 22. Sigel B, Edelstein AL, Felix WR Jr, et al: Compression of the deep venous system of the lower leg during inactive recumbency. Arch Surg 106:38-43, 1973 23. Sigel B, Edklstein AL, Savitch L, et al: Type of compression for reducing venous stasis: A study of lower extremities during inactive recumbency. Arch Surg 110: 171-175,1975

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24. Sigel B, Gibson RJ, Amatneek KV, et al: A Doppler ultrasound method for distinguishing laminar from turbulent flow. A preliminary report. J Surg Res 10:221-224, 1970 25. Sigel B, lpsen J, Felix WR Jr: The epidemiology of lower extremity deep venous thrombosis in surgical patients. Ann Surg 179:278-290,1974 26. Sigel B, Popky GL, Boland JP, et al: Augmentation flow sounds in the ultrasonic detection of venous abnormalities: A preliminary report. Invest Radio1 2:256-258, 1967 27. Sigel B, Popky GL, Mapp EM, et al: Evaluation of Doppler ultrasound examination: Its use in diagnosis of lower extremity venous disease. Arch Surg 100:535-540, 1970 28. Soulen RL, Tyson RR, Reichle FA: Angiographic criteria for small-vessel bypass. Radiology 107 : 5 13-S 19, 1973. 29. Stegall HF, Kardon MB, Kemmerer WT: Indirect measurement of arterial blood pressure by Doppler ultrasonic sphygmomanometry. J Appl Physiol 25:793-798, 1968 30. Strandness DE Jr, Schultz RD, Sumner DS, et al: Ultrasonic flow detection: A useful technique in the evaluation of peripheral vascular disease. Am J Surg 113:3 1l320,1967 31. Sumner DS, Strandness DE Jr: The relationship be-

tween calf blood flow and ankle blood pressure in patients with intermittent claudication. Surgery 65:763771,1969 32. Woodcock JP, Gosling RG, FitzGerald DE: A new non-invasive technique for assessment of superficial femoral artery obstruction. Br J Surg 59:226-231, 1972 33. Yao JS: New techniques in objective arterial evaluation. Arch Surg 106:600604, 1973 34. Yao ST, Gourmos C, Hobbs JT: Detection of proximal-vein thrombosis by Doppler ultrasound flowdetection method. Lancet 1:1-4, 1972 35. Yao ST, Hobbs JT, Irvine WT: Ankle systolic pressure measurements in arterial disease affecting the lower extremities. Br J Surg 56:676-679, 1969