Measurement of arterial blood flow by Doppler ...

Clin. Phys. Physiol. Meas., 1990, Vol. 11, No. 1, 1-26. Printed in the UK

Review article

Measurement of arterial blood flow by Doppler ultrasound L

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P R Hoskins Department of Medical Physics and Medical Engineering, Royal Infirmary, Edinburgh, Scotland, U K Received 10 October 1989, in final form 27 December 1989

Abstract. A review is given of quantitative techniques and clinical applications of arterial Doppler ultrasound. The currently available Doppler equipment of stand-alone continuous wave and pulsed wave units, duplex systems and colour flow systems is briefly described. Doppler ultrasound can be divided into procedures concerned with waveform analysis, volume flow measurement and more recently colour flow imaging. Arterial Doppler waveform analysis is considered for a number of areas including carotid, lower limb, renal and renal transplant, obstetrics, adult cerebral, neonatal cerebral, and tumour studies. Using a duplex scanner volume flow in arteries can be measured from estimates of vessel cross sectional area, mean Doppler frequency and beam-vessel angle. The errors associated with each of these measurements is discussed, and reports of experimentally determined in vivo accuracy of volume flow measurements made using this technique are considered. Other volume flow measurement techniques including the promising attenuation compensation method are also explored.

Contents

1. Doppler effect 2. Instrumentation 2.1. Stand alone continuous wave units 2.2. Duplex systems 2.3. Colour flow 3. Waveform analysis 3.1. Lower limb artery Doppler 3.2. Carotid arteries 3.3. Obstetrics 3.4. Native renal artery 3.5. Transplanted kidney 3.6. Transcranial Doppler 3.7. Neonatal cerebral Doppler 3.8. Tumour studies 4. Volume flow measurement 4.1. Sources of error 4.1.1. Measurement of vessel area 4.1.2. Measurement of beam-vessel angle 4.1.3. Measurement of the component of mean velocity along the Doppler beam 4.1.4. Other effects 4.2. In-vivo measurements of the accuracy of Doppler estimated flow 4.3. Other methods of volume flow measurement 5. Conclusion 0~~3-0815/90/010001 + 26 $03.50

0 1990 Institute of Physical Sciences in Medicine

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P R Hoskins

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1. Doppler effect The change in frequency produced by the scattering of waves by a moving object is a general effect called the Doppler effect. Using ultrasonic equipment the Doppler shift 6F is given by equation (1) below. 6F = 2 f F c o s 0

(1)

where F is the transmitted frequency, v is the velocity of blood, 0 is the beam-vessel angle and c is the speed of sound in tissue. Typically the transmitted frequency is 2 - 8 MHz. In arteries velocities up to 5 or 6 m s - I are present producing Doppler shift frequencies up to about 20 kHz which is just within the audible range. Doppler ultrasound is mostly used to obtain velocity information from moving blood; however, any moving object will produce a Doppler shift. Highamplitude low-frequency signals produced by vessel walls moving during the cardiac cycle are filtered out by a high-pass filter. Occasionally other moving structures such as the fetus produce high amplitude signals which may obliterate the Doppler signal from blood. T h e high attenuation of ultrasound produced by air and bone is in practice not unduly restrictive. Doppler ultrasound signals from many vessels within the body can be obtained using appropriate equipment. In recent years the technique of transcranial Doppler has been developed enabling. Doppler signals to be obtained from intracranial vessels. In this technique some areas of the skull such as the squamous temporal bone are sufficiently thin and uniform to enable passage of an ultrasound beam without severe distortion.

2. Instrumentation 2.1. Stand-alone continuous wave units In these devices a simple pencil probe is used. Continuous wave ultrasound is emitted in a fixed direction by a transmitting element and detected by an adjacent receiving element. T h e Doppler shift signal is extracted and presented in real time as a spectrum (figure 1).

Flgure 1. Doppler spectrum from the common femoral artery obtained using a continuous wave system. The vertical bar indicates the range for 1 kHz.

Arterial Doppler ultrasound

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This is a display of the Doppler frequency shift against time. The Doppler frequency shift is calculated every 5 10 ms. T h e intensity at a particular point is related to the amount of blood within the sample volume moving at the corresponding velocity 'U. The profile of velocities across a vessel which occurs in practice will give rise to a range of Doppler shift frequencies which are visible in the spectrum. The display of the Doppler signal in this way enables the operator to detect easily the presence of artefacts such as interference from underlying or overlying vessels which may be present in the beam. By examining the waveforms the operator can judge when the beam and vessel are properly aligned and when the waveform quality is acceptable. Other methods such as the presentation of a single trace representing the mean or m a x k " frequency are also used; however, the detection of artefacts and of suitable waveform quality is much more difficult using these simple devices. For general usage the display of Doppler blood flow waveforms by real time spectrum analysis has become the method of choice since the introduction of these machines about 10 years ago. Using a stand-alone continuous wave device there is no information supplied by the machine regarding the depth or location of the vessel. This limits the use of these devices to those vessels with well defined locations separate from other vessels, and to those vessels which show well defined waveform shapes. These devices are commonly used in obstetrics to obtain umbilical artery waveforms, and have been widely used for many years in the carotid and lower limb arteries.

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2.2. Duplex systems

A duplex system is a combination of a B-scan device and a Doppler device. An image from a commonly used machine is shown in figure 2. A dotted line along the B-scan image gives the direction of the Doppler beam. T h e use of pulsed Doppler enables blood flow information to be acquired from a known location along the beam. The location is identified by a cursor which can be manually moved along the line. Visualisation of the vessel in

Figure 2 .T h e display h n the internal carotid artery.

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Figure 3. Colour flow images (a)Flow within a diseased internal carotid artery. Calcified plaque on the anterior wall causes shadowing ofthe colour flow image. Contouring of a pre-selected velocity is shown in white. (b)Native kidney showing flow in renal arcuate arteries. Colour flow images by courtesy of Acuson UK Ltd (Stevenage, Hens).

Arterial Doppler ultrasorcnd

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Figure 4. Colour flow images (a) Vessels in the myometrium deep Io the placental. ( h ) Flow in Htd circle of Willis. Colour flow images by courresy of Acuson U K Ltd (Stevenage, Herts).

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P R Hoskins

relation to the direction of the Doppler beam enables the beam-vessel angle to be measured and the spectrum to be calibrated in units of velocity. A number of configurations of duplex system are available commercially. Use of a linear array or phased array allows simultaneous real time B-scanning and display of Doppler waveforms. Simultaneous real-time display using a mechanical sector scanner is more difficult as the B- scan transducer must move in order to update the B-scan, and the vibrations produced are detected by the Doppler device. This usually necessitates switching the Doppler detector off during B-scan update, Stand-alone pulsed Doppler systems, though more commonly used in the past, are now used mainly for transcranial Doppler where imaging of intracranial vessels by a duplex system is difficult.

2.3. Colour jlow Using a duplex system blood flow information is obtained from one particular location within a vessel. A colour flow system combines B-scan imaging with a superimposed real time colour image representing the flow of blood. T h e basic Doppler information presented at a particular point is the mean velocity. Shades of red and blue are usually used to represent velocities away from and towards the transducer. The Doppler signal processor also produces an index called variance based upon the variability over short time periods of the Doppler signal. This quantity is related to the degree of turbulence present in the flow. T h e variance can be displayed separately, typically as a shade of green, or mixed in with the red and blue. Colour flow images from a number of areas of the body are shown in figures 3 and 4.As with duplex systems there are a number of configurations of colour flow systems. Using linear and phased array systems simultaneous real time B-scanning and colour flow Doppler is possible. Using mechanical sector scanning this is more difficult for the reasons mentioned above. The image quality of colour flow systems has improved considerably since their introduction in 1982. Signal processing can be performed to suppress the display of colour on moving tissue, and also to increase the sensitivity to low velocities. Use of a duplex or colour flow system is essential for obtaining Doppler signals when there are a number of closely lying vessels such as in the abdomen or fetus. Further information regarding Doppler physics and instrumentation is given in D H Evans et a1 (1989). 3. Waveform analysis

The Doppler spectrum contains information about the changes in blood velocities over the cardiac cycle. In turn this may be related to the presence of vascular disease. The spectrum is usually used in two ways. Firstly, only the outline, called the maximum frequency envelope (MFE), is used. The absolute value of the frequency shift at a particular point such as peak systole is used for quantitative purposes, or alternatively, indices are derived from the MFE to describe its shape. The second way is to analyse the spectral content of the waveform. The only commonly used feature of spectral content is the spectral broadening index used in carotid artery disease assessment (see section 3.2). The underlying haemodynamics giving rise to the velocity waveform in a particular artery is complex. T h e waveform shape will depend for example on vessel compliance, and any disease, upstream or downstream. The relationship between a particular feature of a Doppler waveform and disease must be investigated separately for each artery and accompanying disease process.


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3.1. Lower limb artery Doppler

Early papers describe the loss of pulsatility of waveforms distal to occlusive vascular disease and the increase in peak velocity in the presence of a stenosis (Strandness et al 1967, Yao et al 1968, Allan and Terry 1969, Fitzgerald et a1 1971). The pulsatility index (PI) was described in terms of Fourier components by Gosling et a1 (1969), but later simplified (Gosling and King 1974) (figure 8). Studies relating PI and changes in PI to disease have been performed in the aorto-iliac segment (Johnston et a1 1978, Baird et a1 1980, Aukland and Hurlow 1982, Baker et a1 1984, McPherson et a1 1984), in the femoro-popliteal segment (Aukland and Hurlow 1982, Baker et al 1986) and in tibial vessels (Aukland and Hurlow 1982). Although major stenoses can be detected, PI is affected by changes in distal arteriolar resistance (Evans et al 1980), and by distal disease (McPherson et ai 1984). More complex methods of analysis have been applied to relate the waveform shape to disease. The Laplace transform (LTD)method was developed by Skidmore and his colleagues (Skidmore and Woodcock 1980a, b, Skidmore et al 1980). In this the waveform shape is derived mathematically from a simple equivalent circuit model of the flow in the lower limb. The expression describing the waveform is fitted to the acquired waveform in the frequency domain (Skidmore and Woodcock 1980a) or the time domain (Law et al 1984) to produce three parameters, wo, y and 6 related to arterial wall elasticity, distal impedance and proximal arterial diameter respectively. This is very attractive in that it appears that the effects of different physiological variables can be isolated, however the validity of the model has been questioned by a number of authors. Several reports have noted the dependency of 6 on peripheral resistance, in contradiction to the model (Evans et a1 1981, Junger et a1 1984, Law et al 1984). The model does not account for the presence of flow throughout the cardiac cycle, which is a feature of proximal disease, but rather constrains the fitted waveform to start at zero flow. The model also does not account for the presence of a shoulder on the downslope of the common femoral artery waveform sometimes seen in the presence of severe superficial femoral artery disease ( D H Evans et al 1989). Both of these points may lead to disagreement between the actual and fitted waveforms. For the prediction by LTD of aorta-iliac stenoses with a diameter greater than 50% some studies report high specificities, at 85% sensitivity (84% by Baird et al (1980), 84% by Johnston et al(1984) and 98% by Baker et al(1989)), however others report very low specificities (2% by MacPherson et al (1984)). Principal component analysis (PCA) is a technique similar to Fourier analysis, in that the waveform shape is broken down into a number of base components of varying shape. In Fourier analysis the base components are sinusoidal, however in PCA the base components are determined by an analysis of the population of waveforms under consideration. The shape of the base components is chosen so that the minimum number of components is needed to reconstruct individual waveforms of the population, typically 2 or 3 components. In the assessment of aortic-iliac disease PI, LTD and PCA were compared by McPherson et al(1984). They found PCA and PI similar, and LTD significantly worse in the classification of mild and severe disease. Campbell et a1 1984 used regression analysis to compare PI, LTD, and PCA. For stenoses less than 50% by diameter LTD performed best whereas PCA and PI contributed little information. For stenoses greater than 50% PCA performed best foll&ed by PI, and LTD contributed little information. These more complex methods have tended to be used primarily as research tools and have not passed into general clinical usage. For lower limb Doppler waveforms possible reasons for this are that these methods are complex 10 implement and offer little improvement over the much simpler pulsatility index.

P R Hoskins

8 3.2. Carotid arteries

Early studies which investigated carotid artery disease can be divided into two groups. In the first group changes in the shape of carotid waveforms characterised by indices such as the ratio of the major systolic peak height to the secondary peak height (AIB ratio) are used (Baskett et a1 1977, Pritchard er a1 1979). In the second group flow in the supraorbital and supratrochlear arteries is investigated (Lo Gerfo and Mason 1974, Bone and Barnes 1976, Keller et aZl976, Baskett et a1 1977, Pritchard et a1 1979, R R Lewis et all984, Padayachee et a1 1984). These arteries communicate between the internal and external carotid circulation, and normally flow is directed outwards from the internal carotid circulation. Carotid disease, particularly internal carotid artery occlusion, may cause reversal of flow direction. Refinements of this test include observation of changes in flow before and after compression of branches of the external carotid artery, and calculation of the A/B ratio. I n general these tests have been reported to be sensitive to major disease, but not minor disease. More recent studies have concentrated on observations of the Doppler spectrum. Blackshear et a1 (1979) and Reneman and Spencer (1979) noted that spectra from the normal internal carotid artery had a clearly defined window underneath the systolic peak, and that disease was associated with an increase in the peak frequency due to increased velocity in the stenosis, and also with filling in of the lower frequencies due to turbulence; that is, spectral broadening. Many studies have compared quantitative indices of spectral broadening with disease classified at arteriography (Johnston er a1 1981, Brown et a1 1982, Rittgers et a1 1983, Sheldon et a1 1983, Johnston et al 1986, Robinson et a1 1988). Sheldon (1985) compared is the most reliable for a number of these indices and demonstrated that F,,IF,,, detection of greater than 40% diameter stenosis; where F,,, and F,,, are the mean and maximum Doppler frequencies respectively at peak systole (figure 5). Disturbed flow

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Figure 5. Variation of the spectral broadening index FmaxlF,,,,,, from the internal carotid artery with degree of stenosis determined angiographically. (Redrawn with permission from Sheldon er a1 1983.)

patterns including flow reversal are known to occur in the normal carotid bifurcation due to the geometry of the bulb (Philips et a l 1983). Morin et a1 (1988) investigated the effect of stenoses on the Doppler spectral content using a model of the carotid birfurcation with continuous flow, and concluded that the flow patterns produced by the normal bulb did not cause spectral broadening except at high flow rates and therefore would be unlikely to be


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confused with spectral broadening caused by disease. Spectral broadening is also affected by the size of the sample volume (van Merode e t al 1983) so will be machine dependent. The measurement of peak frequency shift in the internal carotid artery has been used alone (Johnston et a1 1981, Brown et a1 1982, Sheldon et aI1983), or with reference to peak frequency from the common carotid artery (Keagy et a1 1982, Rittgers e t a1 1983). Using a duplex system allows angle correction and calculation of true velocity (Robinson et a1 1988). These methods are sensitive to major stenoses, but cannot differentiate minor and moderate stenoses from normal (figure 6).

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Figure 6. Variaton of the peak systolic velocity from the internal carotid artery with degree of stenosis determined angiographically. (Redrawn with permission from Robinson et a1 1988.)

A number of studies have used a combination of features of the Doppler waveform including Roederer et al(1982, 1984), Rittgers et a1 (1983), Greene et al(l982) and Langlois er al(1984). The computer based system of Langlois et al (1984) considered 94 candidate features from four sites of which 15 features were selected for use in the classification algorithm, Disease was graded into four categories with an overall accuracy of 83%; the four categories being normal, 1 20% diameter stenosis, 21 50% and 51 99%. Principal component analysis (PCA) has been applied to the maximum frequency envelope of common carotid artery waveforms (Martin et al 1980) where a marginal improvement in performance over the AIB ratio was found, and also to the whole spectrum (Sherriff et a1 1982) where the overall accuracy was 89% for PCA compared to 75% for the AIB ratio. In parallel with the increase in understanding of Doppler spectra from carotid waveforms has been the improvement of real time B-scans. Several recent studies have emphasised the combined use of the B-scan image and Doppler waveform analysis (Hames et al 1985a, b). Cardullo et a2 (1986) in a review of 16 duplex ultrasound papers from 1979 to 1985 found an average accuracy of 91% for classification of disease into greater than 50% diameter stenosis and less than 50% diameter. Colour flow scanning is being used increasingly for arterial Doppler studies and is likely to be particularly suited to the complex flow patterns in carotid arteries (see figure 3(a)).

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3.3. Obstetrics

In the normal. placenta there is a reduction of the resistance to flow throughout pregnancy which is attributed to the continued growth and proliferation of the tertiary stem villi

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(Cohen-Overbeek et a1 1985). Doppler waveforms from the umbilical, utero-placental and fetal arteries have been used to assess the resistance to flow of the placenta; a high resistance indicative of disease being associated with a high pulsatility (figure 7). T h e degree of the

Figure 7. Doppler waveforms from the umbilical cord. T h e vertical bars indicate the range for 1 kHz (a) normal, (h) abnormal.

diastolic flow is characterised by simple indices of the maximum frequency envelope such as resistance index (RI) (Pourcelot 1974) or pulsatility index (PI) (Gosling and King 1974), (figure 8). The basis of this approach came from observational studies made on other arteries where it was noticed that distal vasodilation resulted in increased diastolic flow and loss of pulsatility of the Doppler waveform. In the obstetric field a number of studies have been performed to support this. An increase in the pulsatility of umbilical artery Doppler waveforms was associated with a decrease in the number of small arteries from the terminal villi of the placenta (Giles et al 1985, McCowan et al 1987). Increase in the placental resistance in sheep by embolisation resulted in increased pulsatility of umbilical artery waveforms (Trudinger et a1 1987b, Maulik et al 1989), and of fetal aorta waveforms (Noordam et al 1987). Recently, mathematical modelling of the utero-placental circulation (MOet a1 1988, Adamson er al1989), and of the umbilical circulation (Thomson and Stevens 1989) has been performed. These studies have given further support to this approach.

Figure 8. Definition of pulsnility index (PI) and resistance index

(RI).

In practice a number of technical and physiological factors are known to affect the Doppler waveform. T h e operator should adjust the probe position to obtain Doppler


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waveforms with a clearly defined outline. If the beam-vessel angle is near 90° or if there is substantial offset between the beam and the vessel, the waveform outline will be noisy and indices of RI and PI will be in error. The RI and PI can be falsely elevated if the filter level is set too high, so that end diastolic flow is masked. In practice a level of about 80 Hz or less is desirable. The most important factor affecting feto-placental waveforms is fetal breathing. If this is very strong considerable modulation of the waveforms results (Fouron et al 1975, Hoskins et a l 1988). Other factors such as fetal heart-rate (Mires et aZ 1987, Hoskins et al 1989, van den Wijngaard et al 1989), sampling site along the umbilical cord (Abramawicz et al 1989, Mehalek et al 1989), and behavioural state (van Eyck et al 1985, 1986, 1987, 1988) are known to affect feto-placental waveforms; however, in general, RI and PI are not corrected for these effects. The acquisition of Doppler waveforms from the umbilical cord can be performed using a non-imaging continuous wave system (Fitzgerald and Drumm 1977, Brar et a1 1988), whereas for fetal vessels it is necessary to use a duplex or colour system. Waveforms from the more complex utero-placental circulation have been obtained using continuous wave and duplex systems. Using a duplex system it has been claimed that waveforms can be obtained from the arcuate arteries (Campbell et al 1983), however these vessels are difficult to identify. Using a continuous wave system it is impossible to tell which level of branching is being considered, and it is known that this will affect the pulsatility of the waveforms (Bewley et al 1989, Mehalek et a1 1989). A further error arises because of the similarity between waveforms from the internal iliac artery and abnormal utero-placental waveforms (Pearce and MacParland 1988). Studies have also been performed demonstrating that uteroplacental waveforms have lower pulsatility when taken from the placental side of the uterus (Chambers et el 1988, Kofinas et al 1988, Bewley et al 1989). The use of colour flow for visualisation of utero-placental arteries may help in the establishment of a more reproducible and accurate technique. Many clinical studies have considered the application of Doppler ultrasound to intrauterine growth retardation (IUGR). Early reports using umbilical artery waveforms described the positive association between increased pulsatility and IUGR (Reuwer et al 1984, Erskine and Ritchie 1985a, Fleischer et al 1985, Trudinger et a1 1985b). Later reports have focused on the prediction of fetal compromise (Trudinger et aZ1985a, Reuwer et al 1987, Rochelson et a/ 1987, Laurin et al1987, Haddad et all988, Johnstone et all988). Comparative studies between utero-placental and umbilical (Gudmundsson and Marsal 1988, Mulders et al 1989) and also abdominal circumference measurements (Chambers et al 1989) have been performed. All three studies demonstrated that prediction of fetal compromise was best performed using the umbilical artery (specificities of 80% and 77% respectively for Mulders et al(l989) and Chambers et al(1989) for a sensitivity of 100%) (figure 9). T h e results for utero-placental waveforms were more variable with only Mulders et al(1989) reporting a high specificity (specificities of 64% and 2% respectively for Mulders et al (1989) and Chambers et al(1989) at a sensitivity of 100%). This variability may be associated with the previously discussed difficulty in obtaining utero-placental waveforms from known and reproducible sites. Chambers et aZ(l989) demonstrated that identification of the small-fordates baby using Doppler was poor compared with the standard technique of fetal abdominal circumference measurement using B-scan imaging. In other high risk groups such as diabetics Doppler waveform analysis from the umbilical artery has not been correlated with fetal compromise (Johnston et al, in preparation). This has been attributed to the multifactoral nature of diabetes. T h e use of umbilical artery Doppler waveform analysis in a screening population has been considered by Beattie and Dornan (1989). They considered a number of clinical

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endpoints including centile birthweight for gestation, ponderal index, cord blood p H and packed cell volume, but umbilical waveforms did not adequately predict any of these. Johnstone er al(l989) in a discussion of the paper by Beattie and Dornan (1989) comment that umbilical waveform analysis is perhaps more suited to the prediction of fetal compromise in a high risk population, rather than for use as a screening tool. The use of utero-placental waveform analysis during the second trimester in a screening population has been considered by Campbell et al(1986), Arduini er aZ(l987) and Steel et al(1988). These studies have suggested that patients with abnormal waveforms are more likely to develop hypertensive disorders of pregnancy and IUGR. A number of groups have studied the fetal circulation. Fetal aorta waveform pulsatility was elevated in many cases of IUGR (Joupilla and Kirkinen 1984, Griffin et a1 1984, Tonge et a1 1986). A recent study of fetal renal artery waveforms demonstrated elevated pulsatility in small for gestational age fetuses (Vyas et a1 1989). Waveforms from the fetal internal carotid, middle cerebral, posterior cerebral and anterior cerebral arteries have been acquired (Wladimiroff er al 1986, 1988, Woo et al 1987, Lang et al 1988), and in IUGR the pulsatility of these waveforms decreases. It has been suggested that this is indicative of redistribution of blood flow within the fetus to favour brain blood flow. There has been one small randomised trial of the use of Doppler in obstetrics. Trudinger et a1 (1987a) using umbilical artery waveforms reported that the availability of Doppler measurements reduced the incidence of fetal distress and caesarian section in labour. It is generally perceived that there is insufficient knowledge to justify the widespread use of Doppler in obstetrics (Neilson 1987, Redman 1989), and that further work is needed. 3.4. Native renal artery

Acquisition of Doppler waveforms using duplex scanning of renal arteries and branches of the renal artery can be difficult due to non-visualisation of the vessel and respiratory motion. Technically unsuccessful examination rates of 6 21% have been reported (Greene et a1 1981, Norris et al 1984b). T h e evaluation of renal artery stenosis, by observation of increased frequency and the presence of turbulence, has been reported by a number of

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groups (Norris et a1 1984a, Dubbins 1986, Kohler et a2 1986, Greene et al 1987, Robertson et a l 1988, Taylor et a1 1989). Changes in pulsatility have been used to differentiate obstructive from non-obstructive dilatation (Platt et a2 1989), and to monitor the effect of renovascular dopamine infusion in critically ill patients (Stevens et a1 1989). Pulsatility has also been found to be raised in renal vein occlusion (Dubbins and Wells 1986). 3.5. Transplanted kidney

Assessment of the renal transplant by Doppler has been studied for many years (Sampson 1969, Sampson et a1 1972). These early studies used estimates of blood flow to monitor rejection. Latterly the association between increased pulsatility and rejection has been investigated. Embolisation studies in allografted canine kidneys have shown that increased pulsatility is related to peripheral vascular resistance (Norris and Barnes 1984). Using a porcine model it has been shown that vascular rejection was associated with increased pulsatility in the main, segmental and arcuate renal arteries (Piccirillo et a1 1988), but that similar abnormal Doppler waveforms can also occur as a result of extrarenal compression, renal vein kinking and obstructive uropathy, and that these effects were enhanced by hypotension (Taylor et a1 1988a). A number of studies have demonstrated elevated pulsatility in the presence of acute rejection (Rifkin et a1 1985, Rigsby et a1 1986, Buckley et a l 1987, Murphy e t a1 1987, Needleman and Kurtz 1987, Rifkin et a1 1987, Steinberg et a1 1987, Allen et a1 1988, Fleischer et a1 1989, Genkins et a1 1989, Wan et a1 1989). Some of these studies have noted that elevated pulsatility also occurs in the presence of other pathologies such as acute tubular necrosis, chronic rejection and cyclosporin toxicity. The study by Genkins et al (1989) could demonstrate no correlation of resistance index with the degree of vascular disease within an allograft, or with other pathologies such as acute tubular necrosis and they comment that the pathologic basis for use of resistance index in the assessment of renal allograft malfunction is uncertain. 3.6. Transcranial Doppler

Acquisition of intracerebral artery Doppler waveforms was first described by Aaslid et a1 (1982). Waveforms from the middle cerebral (MCA), anterior cerebral (ACA) and posterior cerebral arteries (PCA) can be acquired through the thin squamous temporal bone, and waveforms from the intracranial portions of basilar and vertebral arteries can be acquired through the foramen magnum (Arnolds and von Reutern 1986). Compression of the common carotid artery may be necessary to identify specific vessels (Aaslid et a1 1982, Arnolds and von Reutern 1986). Acquisition of ACA and PCA waveforms may be difficult as for these vessels a slight angulation of the probe is needed which gives more difficult transmission conditions through the skull (Arnolds and von Reutern 1986, Hennerici et a1 1987). Three-dimensional mapping has been described which allows the operator to map Out the Doppler signals from different arteries in relation to each other (Aaslid 1986, Neiderkon et al 1988). A number of studies have investigated the relationship between the time averaged maximum frequency shift of the Doppler waveform and cerebral blood flow. MCA timeaveraged maximum frequency has been found to relate closely to the arterial carbon dioxide tension both within and between subjects (Kirkham et aIl986). In this study carbon dioxide tension was used as an index of flow. Comparison of time averaged maximum frequency shift with regional blood flow measured by xenon clearance showed poor correlation (Bishop et a1 1986, Halsey er a1 1989). Halsey et a1 (1989) suggested that one factor contributing to this could be the fact that these two methods do not measure flow to

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comparable parts of the brain. Assessment of carbon dioxide reactivity by regional blood flow and Doppler in the MCA gave good correlation (Bishop et a1 1986). There are a number of assumptions implicit in the use of a velocity estimate as an index of flow, including the assumption that the diameter of a particular vessel is fixed and identical for all patients, that the angle is near to zero, and that there is a fixed relationship between the mean and maximum velocities. This has lead to comments of care in the use and interpretation of velocity estimates as indices of flow (Kontos 1989). The pulsatility of the Doppler waveform has also been used. Klingelhofer et al(l988) obtained good correlation between intracranial pressure and the quantity (mean systemic arterial pressure) x (resistance index)l(mean flow velocity) from the MCA. Hassler er a1 (1988) also noted that raised intracranial pressure was associated with increased pulsatility of the MCA. T h e effect of haemotocrit on peak velocity and pulsatility was investigated by Brass et a1 (1988) who suggested that both these quantities may need correction in the presence of anaemia. Clinical studies which have been performed include the diagnosis and follow-up of vasospasm in the MCA after subarachnoid haemorrhage (Aaslid e t a1 1984, Sieler et a2 1986), and for monitoring the MCA during carotid endarterectomy (Padayachee et al 1986, 1987) and cardiopulmonary bypass surgery (Lundar et a1 1985, von Reutern et a1 1988). 3.7. Neonatal cerebral Doppler

Bada et al (1979) were the first to report Doppler waveform acquisition from neonatal intracerebral vessels. They obtained anterior cerebral artery waveforms through the anterior fontanelle. A duplex system can be used to obtain waveforms from other vessels imaged through the fontanelle, and middle cerebral artery waveforms may be obtained using transcranial Doppler techniques. Both the waveform pulsatility and indices of velocity such as the time averaged maximum velocity can be used to characterise the Doppler waveform. Changes in waveforms have been reported in many conditions including periventricular haemorrhage (Bada er al 1979, Perlman and Volpe 1982), asphyxia (Bada et a1 1979, Evans et a1 1985), seizures (Perlman et al1983), pneumothorax (Hill et a l l 9 8 2 ) and hydrocephalus (Hill and Volpe 1982, Seibert et al 1989). In recent reviews of neonatal cerebral Doppler, Archer and Evans (1988) and Drayton and Skidmore (1986) comment that in some conditions the waveform abnormalities will be primarily as a result of disturbances in cardiac output and blood pressure. In other areas of the body waveform pulsatility is related to downstream resistance to flow. In their review of the literature Archer and Evans (1988) conclude that the relationship between resistance index (RI) and neonatal cerebral vascular resistance is unclear, and that RI appears to correlate poorly or not at all with cerebral blood flow. There is some evidence that velocity indices correlate with cerebral blood flow (Batton er a1 1983, Hansen et a1 1983, Greison et a1 1984), and Archer and Evans (1988) comment that velocity indices may be of more value than RI in following blood flow changes, however, as with transcranial applications (section 3.6.) the relationship between Doppler frequencies and blood flow is complex, which should lead to caution in the interpretation of changes in the Doppler derived flow estimate. D H Evans er a1 (1989) comment that much of the value of neonatal cerebral Doppler may lie in helping to elucidate the pathophysiology of various intracranial abnormalities rather than as a clinical tool. 3.8. Tumour studies The first reported use of Doppler ultrasound in this area was by Wells et al (1977) who studied lumps in the breast. Doppler signals from neovascular tumours typically show high


15

frequency shifts and low pulsatility, associated with the presence of arteriovenous anastomoses within the tumour. These features have been observed in waveforms from tumours of the breast (Burns et al 1982, Minasian and Bamber 1982, Srivastava et a1 1988), kidney (Ramos et a1 1988, Kuijpers and Jaspers 1989), thyroid (Woodcock et al1985), liver, adrenal glands and pancreas (Taylor et a1 1988b). Most studies in this area have used continuous wave or duplex systems, however colour flow is likely to be increasingly used as large volumes of tissue can be rapidly interrogated for blood flow signals. A more detailed discussion of the application of Doppler ultrasound to tumour flow is given in Wells (1989). 4. Volume flow measurement Using a duplex system the possibility arises of measuring volume flow in blood vessels. Volume flow is the product of cross-sectional area and mean velocity. T h e vessel area is estimated from the B-scan, and the mean velocity is estimated from the mean frequency shift of the Doppler spectrum and the beam-vessel angle, equation (2): Mean velocity

c

=26FX -

Mean frequency shift

case

In the literature volume flow in a large number of vessels has been measured, including the common femoral artery (Lewis er a1 1986), common carotid artery (Uematsu er a1 1983), superior mesenteric artery (Aldoori et al 1985), renal artery (Reid et al 1980, Greene et al 1981, 1986), in the adult aorta for determination of cardiac output (see section 4.2) and in the fetal aorta (Eik-Nes er a1 1980, Griffin et a1 1985, Erskine and Ritchie 1985b). The errors associated with measurement of volume flow using a duplex scanner are considered in sections 4.1 and 4.2 below. Alternative techniques of volume flow measurement are considered in section 4.3. 4.1. Sources of ertor

Detailed discussion of errors is given in Gill (1985), Evans (1986) and D H Evans et a1 (1989). The main sources of error are discussed below. 4.1.1. Measurement of vessel area. The usual method of area measurement is to measure diameter and calculate area from nd2/4. A fractional error E in diameter measurement gives an error 2E in area measurement. The best achievable accuracy will be of the order of a wavelength of the imaging system, larger errors being associated with smaller diameters. A typical frequency of 5 MHz has a wavelength of 0.3 mm. For a diameter of 10 mm the associated theoretical error in area will be about 670, for 5 mm it will be 12% and for 3 mm it will be 20% (see Evans 1986). In practice these best errors will be increased by the difficulty in defining the vessel wall in the scan, especially if there is disease present, and the fact that the artery pulsates which can change the diameter by up to 10%.

4.1.2. Measurement of angle. This is measured by aligning a cursor with the vessel wall. The error introduced by incorrect measurement of angle increases as the angle increases. For example an error of _t3" for an angle of 30" gives rise to a 3% error in flow, whereas the same error in angle at 70" gives a 15% error in flow (see Evans 1986). It should also be noted that for angles approaching 90" the simple cos@ dependence of frequency shift is not obeyed. Geometrical spectral broadening (Newhouse er a1 1987) acts to give a non-zero Doppler shift at 90". In practice this is unlikely to be of concern.

P R Hoskins

16

4.1.3. Measurement of the component of mean velocity along the DoppIer beam. If the vessel is uniformly insonated the mean frequency shift will be proportional to the component of mean velocity along the Doppler beam. In general non-uniform insonation leads to overestimation of the mean velocity as the low velocity components present at the edge of the vessels are ignored. For continuous flow Evans (1986) has performed theoretical calculations on the degree of overestimation of the mean velocity using a rectangular beam profile. For a beam width which is 50% of the vessel diameter the error in flow is about 22%. For a width of 20% the error is 32%. 4.1.4 Other effects. So far it has been assumed that flow is laminar. When arterial disease is present this can give rise to varying degrees of non-laminar flow. In these situations the blood moves in all directions with respect to the Doppler beam so that a single beam vessel angle is no longer meaningful. Measurements of flow in these circumstances are likely to be in error. Further effects may need to be accounted for such as the use of a high pass filter (Gill 1979), and the change in centre frequency produced by frequency dependent attenuation (Holland et aI 1984). 4.2. In-vivo measurements of the accuracy of Doppler estimated fIow There is little published information on the accuracy of volume flow measurement using ultrasound in vivo. Most reports in this area compare the Doppler estimated flow and the gold standard flow by fitting a least squares regression line and quoting the correlation coefficient, line slope and intercept. In order to compare various studies, where possible the difference between the Doppler estimated flow and the gold standard flow has been estimated to give an absolute percentage error, and for each group of measurements the root mean square (RIMS) error has been calculated from the absolute percentage errors. Table 1 shows the results of this analysis. There is a wide range of RMS errors from 9% to 101%. Table 1. Accuracy of Doppler estimates of volume flow compared against gold standard estimates of flow by electromagnetic flowmetry (EMF), Fick technique (Fick) and thermodilution technique (TD). Fick and TD refer to cardiac output measurements only. Of the 15 studies 13 used a duplex system to measure flow. The studies by J M Evans et a/(1989b) and Looyenga et ai (1989) used the attenuation compensation technique, and these are shown for comparative purposes. Study

Animal Flow measurement

Eik-Nes et a/(1984) Pig Dog Avasthi er a/ (1984) Sheep Struyck er a/ (1 985) Walter er ai (1986) Dog Dog Walter er a/(1986) Man Magnin et a/ (1981) Goldberg et a/ (1 982) Man Meijboom et a/ (1983) Dog Huntsman et a/ (1983) Man Valdes-Cruz er a / (1983) Dog Man Ihlen et ai (1984) Man Ihlen et ai (1984) J F Lewis et ai (1984) Man J M Evans et ai (1989b)*Man Looyenga er a/ (1989)* Man ~

Abdominal aorta Renal artery Descending aorta Abdominal aorta Femoral artery Cardiac outpur Cardiac output Cardiac output Cardiac ourput Cardiac output Cardiac output Cardiac outpur Cardiac output Cardiac output Cardiac ourput

~~

Attenuation compensation method

Gold standard EMF EMF EMF EMF EMF

Fick TD

EMF TD

EMF TD

Fick TD TD

TD

n 18 35 3 12 12 11 10 26 110 32 20 10 35 54 71

Absolute error (To)

RMS error (To)

0 IO 26 -56 to 160 -7.5 10 17 80 to 149 - 2 10 46 -68 to 0 -40 to 47 -26 to 24 17 10 66 -23 to 47 -14 to 35 -36 to 13 -70 to 40 -24 to 29 -31 to 25

11 44 11 101 34 34 25 11 9 16 12 24 24 11 10

-


17

For estimation of cardiac output the average RMS error is 19%. This range of errors emphasises the difficulty in measuring volume flow and may help explain why commonly used routine estimates of volume flow using a duplex system are not performed.

4.3. Other methods of volume flow measurement Variations of the above method for measurement of volume flow have been described including multigate devices for velocity profile measurement, and devices which attempt to measure the angle by combining or comparing the output from two or more Doppler transducers. These methods are described in D H Evans et al (1989). Commercial devices using these systems are not commonly available. A technique of volume flow measurement currently under assessment is that of attenuation compensation. This technique combines Doppler power measurements and mean frequency measurements. This was first described by Hottinger and Meindl (1979) and has been applied to the measurement of cardiac output by J M Evans et aZ(1989a, b). A dual element annular array is used. First measurements of power and mean frequency are made using the small central transducer. This gives uniform insonation of the aorta. Secondly the combined dual element device is used to produce a narrow beam so that the sample volume is located entirely within the aorta. Combination of these power and mean frequency measurements results in volume flow without the need to measure the angle or the cross sectional area of the vessel. Comparison of this technique with thermodilution flow measurement indicates good agreement (J M Evans et a1 1989b, Looyenga et a1 1989) (figure lo), with an RMS error of 10 to 11% (table 1).

/ o r 0

I

I

,

*

4 6 8 10 12 14 16 Thermodilution flow rate (I min.') Figure 10. Cardiac output determined by thermodilution and by the attenuation compensation method. (Reprinted with permission from J M Evans et al 1989b.) 2

The measurements of volume flow considered above use transcutaneous techniques. Doppler ultrasound flowmeters have also been described for intraoperative measurement of arterial flow (Beard et al 1986, Richardson et a1 1987, Cowan et a1 1988). In these devices the artery is constrained in a solid cuff which also houses the Doppler transducer at a fixed angle with respect to the artery. In this way there is a fixed geometrical relationship between the artery and the transducer beam, and correction factors can be applied in the estimation of mean velocity to help account for partial insonation of the vessel. The flow error in most vessels of interest is less than lo%, however Beard et a1 (1986) note that for vessels with

18

P R Hoskins

an internal diameter of 2 mm or less the error is likely to approach 20% unless the internal diameter can be accurately measured. There are a number of features of the Doppler ultrasound flowmeter which may make it more suitable for routine intraoperative flow measurement than the electromagnetic flowmeter, including the absence o f electrical contact with the vessel, and reduced problems of calibration. The use of a Doppler ultrasound flowmeter in the assessment of femorodistal bypass grafts has recently been reported by Beard er al (1989).

5. Conclusion Doppler information from a wide range of arteries in the body can be obtained using a variety of equipment. The Doppler waveform pattern is often a result of complex underlying physical, physiological and pathological processes. T h e current understanding of the interpretation and clinical use of Doppler waveforms in particular areas is often the result of research over a period of many years. Volume flow measurement also cannot be performed without due care and attention to the underlying sources of error. The ease with which flow may be visualised using colour flow Doppler is likely to make this technique increasingly important in routine clinical practice. Acknowledgements Thanks to Mrs A McMillan and Mrs D Nicholson for typing the manuscript. Thanks to Professor W N McDicken, Dr P Allan, Dr S E Chambers, Dr F D Johnstone, D r S Pye and Dr R Seller for helpful discussions and suggestions. This review is based on a lecture given at a Biomedical Research Seminar on Quantitative Imaging In Vivo at the Royal College of Physicians of Edinburgh, and I would like to thank Professor Mallard for inviting me to speak at that meeting. I acknowledge the financial support provided by Acuson UK Ltd (Stevenage, Herts) which has enabled colour illustrations to be printed in this review. References Aaslid R 1986 Transcranial Doppler Sonography (Vienna/New York: Springer-Verlag) Aaslid R, Huber P and Nornes H 1984 Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound J . Neurosurg. 60 37-4 1 Aaslid R, Markwalder T M and Nornes H 1982 Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries J. Neurosurg. 57 769-74 Abramawicz J S, Warsof S L, Arrington J and Levy D L 1989 Doppler analysis of the umbilical artery: the importance of choosing the placental end of the cord J . Ultrasound Med. 8 219-21 Adamson S L, Morrow R J, Bascom P A J, MO L Y L and Ritchie J W K 1989 Effect of placental resistance, arterial diameter and blood pressure on the uterine arterial velocity waveform: a computer modelling approach Ultrasound Med. Biol. 15 437-42 Aldoori M I, Qamar M I, Read A E and Williamson R C N 1985 Increased flow in the superior mesenteric artery in,dumping syndrome Br. J. Surg. 7 2 389-90 Allan J S and Terry H J 1969 T h e evaluation of an ultrasonic flow detector for the assessment of peripheral vascular disease Cardiovasc. Res. 3 503-9 . Allen K S, Jorkasky D K, Arger P H, Velchik M G, Grumbach K, Coleman B G, Mintz M C, Betsch S E and Perloff L J 1988 Renal allografts: prospective analysis of Doppler sonography Radiology 169 371-6 Archer L N J and Evans D H 1988 Doppler assessment of the neonatal cerebral circulation Fetal and Neonatal Neurology and Neurosurgery eds M I Levene, M J Bennett and J Punt (Edinburgh: Churchill-Livingstone) p p 162-8


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Arduini D, Rizzo G, Romanini C and Mancuso S 1987 Utero-placental blood flow velocity waveforms as predictors of pregnancy-induced hypertension Eur. J . Obstet. Gynecol. Reprod. B i d 26 335-41 Arnolds B J and Reutern G M von 1986 Transcranial Doppler sonography. Examination technique and normal reference values Ultrasound Med. Bid. 12 115-23 Auckland A and Hurlow R A 1982 Spectral analysis of Doppler ultrasound: its clinical application in lower limb ischaemia Br. J . Surg. 6 539-42 Avasthi P S, Greene E R, Voyles W F and Eldridge M W 1984 A comparison of echo-Doppler and electromagnetic renal blood flow measurements J . Ultrasound Med. 3 213-8 Bada H S, Hajjar M S, Chua C and Sumner D S 1979 Noninvasive diagnosis of neonatal asphyxia and intraventricular haemorrhage by Doppler ultrasound J. Pediatr. 95 775-9 Baird R N, Bird D R, Clifford P C, Lusby R J, Skidmore R and Woodcock J P 1980 Upstream stenosis diagnosed by Doppler signals from the femoral artery Arch. Surg. 115 1316-22 Baker A R, Prytherch D R, Evans D H and Bell P R F 1986 Doppler ultrasound assessment of the femoropopliteal segment: comparison of different methods using ROC analysis Ultrasound Med. Biol. 12 473-82 Baker J D, Machleder H I and Skidmore R 1984 Analysis of femoral artery Doppler signals by Laplace transform damping method J. Vasc. Surg. 1 520-4 Baker J D, Skidmore R and Cole S E A 1989 Laplace transform analysis of femoral artery Doppler signals: the state of the art Ultrasound Med. Biol. 15 13-20 Baskett J J, Beasley M G, Murphy G J, Hyams D E and Gosling R G 1977 Screening for carotid junction disease by spectral analysis of Doppler signals Cardiovasc. Res. 11 147-55 Batton D G, Hellmann J, Hernandez M J and Maisels M J 1983 Regional cerebral blood flow, cerebral blood velocity and pulsatility index in newborn dogs Pediatr. Res. 17 908-12 Beard J D, Evans J M, Skidmore R and Horrocks M 1986 A Doppler flowmeter for use in theatre Ultrasound Med. B i d . 12 883-9 Beard J D, Scott D J A, Skidmore R, Baird R N and Horrocks M 1989 Operative assessment of femorodistal bypass grafts using a new Doppler flowmeter Br. J. Surg. 76 925-8 Beattie R B and Dornan J C 1989 Antenatal screening for intrauterine growth retardation with umbilical artery ultrasonography Br. Med. J . 298 631-5 Bewley S, Campbell S and Cooper D 1989 Uteroplacental Doppler flow velocity waveforms in the second trimester: a complex circulation Br. J . Obstet. Gynaecol. 96 1040-6 Bishop C C R, Powell S, Rutt D and Browse N L 1986 Transcranial Doppler measurement of middle cerebral artery blood flow velocity: a validation study Stroke 17 913-5 Blackshear W M, Philips D J, Thiele B L, Hirsch J H, Chikos P M, Marinelli M R, Ward K J and Strandness D E 1979 Detection of carotid occlusive disease by ultrasonic imaging and pulsed Doppler spectrum analysis Surgery 86 698-706 Bone G E and Barnes R W 1976 Limitations of the Doppler cerebrovascular examination in hemispheric cerebral ischaemia Surgery 79 577-80 Brar H S, Medeoris A L, De Vore G R and Platt L D 1988 Fetal umbilical velocimetry using continuous wave and pulsed wave Doppler ultrasound in ultrasound in high risk pregnancies: a comparison of systolic to diastolic ratios Obsta. Gynecol. 72 607-10 Brass L M, Pavlakis S G, De Vivo D, Piomelli S and Mohr J P 1988 Transcranial Doppler measurements of the middle cerebral artery. Effect of hematocrit Stroke 19 1466-9 Brown P M, Johnston K W, Kassam M and Cobbold R S C 1982 A critical study of ultrasound Doppler spectral analysis for detecting carotid disease Ultrasound Med. Biol. 8 515-23 Buckley A R, Cooperberg P L, Reeve C E and Mogil A B 1987 The distinction between acute renal transplani rejection and cyclosporine nephrotoxicity: value of Doppler sonography Am. J. Roentgenol. 149 521-5 Burns P N,Halliwell M, Wells P N T and Webb A J 1982 Ultrasonic Doppler studies of the breast Ultrusound Med. B i d . 8 127-43 Campbell S, Diaz-Recasens J, Griffin D R, Cohen-Overbeck T E, Pearce J M, Willson K and Teague M J 1983 New Doppler technique for assessing uteroplacental blood flow Lancer i 675-7 Campbell S, Pearce J M F, Hackett G, Cohen-Overbeck T and Hernandez C 1986 Qualitative assessment of uteroplacental blood flow: early screening test for high risk pregnancies Obstet. Gynecol. 68 649-53 Campbell W B, Cole S E A, Skidmore R and Baird R N 1984 T h e clinician and the vascular laboratory in the diagnosis of aorta- iliac stenosis Br. J. Surg. 71 302-6 Cardullo P A, Cutler B S and Wheeler H B 1986 Detection of carotid artery disease by duplex ultrasound J. Diug. Med. Sonog. 2 63-73 Chambers S E, Hoskins P R, Haddad N G, Johnstone F D, McDicken W N and Muir B B 1989 A comparison of fetal abdominal circumference measurements and Doppler ultrasound in the prediction of small-for-dates babies and fetal compromise Brit. J. Obstet. Gynaecol. 96 803-8

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Chambers S E, Johnstone F D, Muir B B, Hoskins P R, Haddad N G and McDicken W N 1988 The effects of placental site on the arcuate artery flow velocity waveform J . Ultrasound Med. 7 671-3 Cohen-Overbeek T, Pearce J M and Campbell S 1985 The antenatal assessment of utero-placental and fetoplacental blood flow using Doppler ultrasound Ultrasound Med. Biol. 11 329-39 Cowan D, Stevens A L and Roberts V C 1988 Design of a continuous-wave Doppler ultrasonic flowmeter for perivascular applications Part 2: Signal processing system Med. Biol. Eng. Comput. 26 153-60 Drayton, M R and Skidmore, R 1986 Doppler ultrasound in the neonate Ultrasound Med. Biol. 12 761-72 Dubbins P A 1986 Renal artery stenosis: duplex ultrasound examination Br. J. Radiol. 59 225-9 Dubbins P A and Wells I 1986 Renal carcinoma: duplex Doppler examination Br. J. Radiol. 59 231-6 Eik-Nes S H, Brubakk A 0 and Ulstein M K 1980 Measurement of human fetal blood flow Br. Med. J . 280 283-4 Eik-Nes S H, Marsal K and Kristofferson K 1984 Methodology and basic problems related to blood flow studies in the human fetus Ultrasound Med. Biol. 10 329-37 Erskine R L A and Ritchie J W K 1985a Quantitative measurement of fetal blood flow using Doppler ultrasound Br. J . Obstet. Gynaecol. 92 600-4 1985b Umbilical artery blood flow characteristics in normal and growth-retarded fetuses Brir. J. Obstet. Gynecol. 92 605-10 Evans D H 1986 Can ultrasonic duplex scanners really measure volumetric flow? Physics in Medical Ultrasound Ed J 4 Evans (York: IPSM) pp 145-54 Evans D H, Archer L N J and Levene M I 1985 The detection of abnormal neonatal cerebral haemodynamics using principal component analysis of the Doppler ultrasound waveform Ultrasound Med. Biol. 11 441-9 Evans D H, Barrie W W, Asher M J, Bentley A S and Bell P R F 1980 T h e relationship between ultrasonic pulsatility index and proximal arterial stenosis in a canine model Circ. Res. 46 470-5 Evans D H, Macpherson D S, Bentley S, Asher M J and Bell P R F 1981 The effect of proximal stenosis on Doppler waveforms: a comparison of three methods of waveform analysis Clin. Phys. Physiol. Meas. 2 17-25 Evans D H, McDicken W N, Skidmore R and Woodcock J P 1989 Doppler Ultrasound: Physics, Instrumentation and Clinical Applications (Chichester: John Wiiey) Evans J M, Skidmore R, Luckman N P and Wells P N T 1989a A new approach to the noninvasive measurement of cardiac output using an annular array Doppler technique I - Theoretical considerations and ultrasonic fields Uftrasound Med. Biol. 15 169-78 Evans J M, Skidmore R, Baker J D and Wells P N T 1989b A new approach to the noninvasive measurement Practical implementation and results of cardiac output using an annular array Doppler technique I1 Ultrasound Med. Biol. 15 179-87 Eyck J van, Wladimiroff J W, Noordam M J, Tonge H M and Prechtl H F R 1985 The blood flow velocity waveform in the fetal descending aorta: its relationship to fetal behavioural states in normal pregnancy at 37-38 weeks Early Hum. Dev. 12 137-43 -1986 The blood flow velocity waveform in the fetal descending aorta: its relationship to behavioural states in the growth retarded fetus at 37-38 weeks of gestation Early Hum. Dev. 14 99-107 Eyck J van, Wladimiroff J W, Noordam M J, Wijgaard J A G W van der and Prechtl H F R 1988 The blood flow velocity waveform in the fetal internal carotid and umbilical artery; its relation to fetal behavioural states in the growth retarded fetus at 37-38 weeks gestation Br. J . Obster. Gynaecol. 95 473-7 Eyck J van, Wladimiroff J W, Wijgaard J A G W van der, Noordam M J and Prechtl H F R 1987 The blood flow velocity waveform in the fetal internal carotid and umbilical artery; its relation to fetal behavioural states in normal pregnancy at 37-38 weeks Br. J. Obsret. Gynaecol. 94 736-41 Fitzgerald, D E and Drumm, J E 1977 Non-invasive measurement of the fetal circulation using ultrasound; a new method Br. Med. J. 2 1450-1 Fitzgerald D E, Gosling R G and Woodcock J P 197 1 Grading dynamic capability of arterial collateral circulation Lancet i 66-7 Fleischer A, Schulman H, Farmakides G, Bracero L, Blattner P and Randolph G 1985 Umbilical artery velocity waveforms and intra-uterine growth retardation A m . J. Obster. Gynecol. 151 502-5 Fleischer A C, Hinton A A, Glick A D and Johnson H K 1989 Duplex Doppler sonography of renal transplants: correlation with histopathology J. Ultrasound Med. 8 89-94 Fouron J, Korcaz Y and Leduc B 1975 Cardiovascular changes associated with fetal breathing A m . J . Obster. Gynecol. 123 868-76 Genkins S M,Sanfilippo F P and Carroll B A 1989 Duplex Doppler sonography of renal transplants: lack of sensitivity and specificity in establishing pathologic diagnosis A m . J. Roenrgenol. 152 535-9 Giles W B, Trudinger B J and Baird P J 1985 Fetal umbilical artery flow velocity waveforms and placental resistance: pathological correlation Br. J. Obsret. Gynaecof. 92 3 1-8 Gill R W 1979 Pulsed Doppler with B-mode imaging for quantitative blood flow measurement Ultrasound Med. Biof. 5 223-5

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21

Gill R W 1985 Measurement of blood flow by ultrasound: accuracy and sources of error Ultrasound Med. Biol. 11 625-41 Goldberg S J, Sahn D J, Allen H D, Valdes-Cruz L M, Hoenecke H and Carnaham Y 1982 Evaluation of pulmonary and systemic blood flow by 2-dimensional Doppler echocardiography using fast Fourier transform spectral analysis A m . J . Cardiol. 50 1394-400 Gosling R G and King D H 1974 Continuous wave ultrasound as an alternative and complement to X-rays in vascular examination Cardiovascular Applications of Ultrasound Ed R S Reneman (Amsterdam: North Holland) pp 266-82 Gosling R G , King D H, Newman D L and Woodcock J P 1969 Transcutaneous measurement of arterial blood velocity ultrasound Ultrasonics for Industry Conference Papers (Guildford: IPC) pp 16-32 Greene E R, Avasthi P S and Hodges J W 1987 Nonvasive Doppler assessment of renal artery stenosis and hemodynamics J. Clin. Ultrasound 15 653-9 Greene E R, Avasthi P S, Voyles W F and Seigel R 1986 Noninvasive versus invasive Doppler renal blood velocity and flow measurements I E E E Trans. Biomed. Eng. BME-33 302-7 Greene E R, Venters M D, Avasthi P S, Conn R L and Jahnke R W 1981 Noninvasive characterisation of renal artery blood flow Kidney Int. 20 523-9 Greene F M, Beach K, Strandness D E, Fell G and Philip D J 1982 Computer based pattern recognition of carotid arterial disease using pulsed Doppler ultrasound Ultrasound Med. Biol. 8 161-76 Greisen G, Johansen K, Ellison P H, Fredenksen P S, Mali J and Friis-Hansen B 1984 Cerebral blood flow in the newborn infant: comparison of Doppler ultrasound and 133-Xenon clearance J. Pediatr. 104 41 1-8 Griffin D R, Bilardo K, Masini L, Diaz-Recasens J, Pearce J M, Willson K and Campbell S 1984 Doppler blood flow waveforms in the descending thoracic aorta of the human fetus Br. J, Obster. Gynaecol. 91 997-1006 Griffin D R, TeagueM J, Taller P, Willson K, Bilardo C, Massini L and Campbell S 1985 A combined ultrasonic linear array scanner and pulsed Doppler velocimeter for the estimation of blood flow in the foetus and adult abdomen I1 Clinical evaluation Ultrasound Med. Biol. 11 37-41 Gudmundsson S and Marsal K 1988 Umbilical and uteroplacental blood flow velocity waveforms in pregnancies with fetal growth retardation Eur. J. Obsta. Gynecol. Reprod. Biol. 27 187-96 Haddad N G , Johnstone F D, Hoskins P R, Chambers S E, Muir B B and McDicken W N 1988 Umbilical artery Doppler waveforms in pregnancies with uncomplicated intra-uterine growth retardation Gynecol. Obszer. Invest. 26 206-10 Halsey J H, McDowell H A, Gelman S and Morawetz R B 1989 Blood velocity in the middle cerebral artery and regional cerebral blood flow during carotid endarterectomy Stroke 20 53-8 Hames T K, Humphries K N, Ratliff D A, Birch S J, Gazzard V M and Chant A D B 1985a The validation of duplex scanning and continuous wave Doppler imaging: a comparison with conventional angiography Ultrasound Med. Biol. 11 827-34 Hames T K, RatliffD A, Humphries K N, Gazzard V M, Birch S J and Chant A D B 1985b The accuracy of duplex scanning in the evaluation of early carotid disease Ultrasound Med. Biol. 11 819-25 Hansen N B, Stonestreet B S, Rosenkrantz T S and Oh W 1983 Validity of Doppler measurements of anterior cerebral artery blood flow velocity: correlation with brain blood flow in piglets Pediatrics 72 526.31 Hassler W, Steinmetz H and Gawlowski J 1988 Transcranial Doppler ultrasonography in raised intracranial pressure and in intracranial circulatory arrest J . Neurosurg. 68 745-51 Hennerici M, Routerberg W, Sitzer G and Schwartz A 1987 Transcranial Doppler ultrasound for the assessment part I examination technique and normal values Surg. Neurol. of intracranial arterial flow velocity 27 439-48 Hill A, Perlman J M and Volpe J J 1982 Relationship of pneumothorax to occurrence of intraventricular hemorrhage in the premature newborn Pediatrics 69 144-9 Hill A and Volpe J J 1982 Decrease in pulsatile flow in the anterior cerebral artery in infantile hydrocephalus Pediatrics 69 4-7 Holland S K, Orphanoudakis S C and Jaffe C C 1984 Frequency dependent attenuation effects in pulsed Doppler ultrasound: experimental results IEEE Trans. Biomed. Eng. BME-31 626-3 1 Hoskins P R, Johnstone F D, Chambers S E, Haddad N G , White G and McDicken W N 1989 Heartrate variation of umbilical artery Doppler waveforms Ultrasound Med. Biol. 15 101-5 Hoskins P R, McDicken W N, Johnstone F D, White G, Haddad N G and Chambers S E 1988 Determination of the presence of fetal apnoea using umbilical artery and umbilical vein Doppler waveforms Ulrrasound Med. Bioi. 14 589-92 Hottinger C F and Meindl J D 1979 Blood flow measurement using the attenuation-compensated volume flowmeter Ultrasonic Imaging 1 1-15 Huntsman L L, Stewart D K, Barnes S R, Franklin S B, Colocousis J S and Hessel E A 1983 Noninvasive Doppler determination of cardiac output in man; clinical validation Circulation 67 593-602

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Ihlen H, Amlie J P, Dale J, Forfang K, Nitter-Hauge S, Otterstad J E, Simonsen S and Myhre E 1984 Determination of cardiac ourput by Doppler echocardiography BY. Heart J . 51 54-60 Johnston K W, Baker W H, Burnham S J, Hayers A C, Kupper C A and Poole M A 1986 Quantitative analysis of continuous wave Doppler spectral broadening for the diagnosis of carotid disease: results of a multicenter study J . Vasc. Surg. 4 493-504 Johnston K W, Kassam M, Koers J, Cobbold R S C and MacHattie 1984 Comparative study of four methods for quantifying Doppler ultrasound waveforms from the femoral artery Ultrasound Med. Biol. 10 1-12 Johnston K W, Maruzzo B C and Cobbold R S C 1978 Doppler methods for quantitative measurement and localisation of peripheral arterial occlusive disease by analysis of the blood flow velocity waveform Ultrasound Med. 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