Pattern of Doppler Flow Indices at the Carotid Bifurcation

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1 Article Pattern of Doppler Flow Indices at the Carotid Bifurcation Evaluation by Hemodynamic Color Doppler Imaging G. Sharat Lin, PhD, Veena S. Naval, MA Objective. To visualize the spatial variation of Doppler indices, principally the pulsatility index, taken proximal to the carotid bifurcation and to evaluate their relationship to the geometry of the carotid bulb. Methods. The pattern of ultrasonographic Doppler indices was studied in healthy volunteers by using hemodynamic color Doppler imaging, which computes and displays a Doppler index at each color pixel from a sequence of color Doppler image frames taken over several cardiac cycles. Results. In carotid bulbs with laminar flow (n = 5), the spatial partitioning between low-resistance internal carotid artery and high-resistance external carotid artery flows could be followed over 5 cm upstream in the common carotid artery. However, normal reverse or vortex flows at the carotid bulb (n = 15) obliterated upstream flow partitioning within 2 cm of the flow divider. The pulsatility index was neither laterally nor axially uniform in the common carotid artery. Conclusions. Localization of core flow where meaningful Doppler indices may be measured is determined by the expansion geometry of the carotid bulb and usually requires positioning of a small sample volume in the center of the lumen at least 3 cm upstream from the flow divider. However, in the absence of reverse or vortex flows, placement of a spectral Doppler sample volume is best guided by hemodynamic color Doppler imaging. Key words: carotid arteries; color Doppler ultrasonography; pulsatility index; carotid bifurcation; blood flow dynamics; flow reversal. Abbreviations CCA, common carotid artery; CDI, color Doppler imaging; ECA, external carotid artery; HCDI, hemodynamic color Doppler imaging; ICA, internal carotid artery; PI, pulsatility index; RI, resistance index; S/D, systolicdiastolic ratio Received May 16, 2001, from Advanced Imaging Associates, Fremont, California. Revision requested June 12, Revised manuscript accepted for publication September 10, This research was supported by equipment provided by GE Medical Systems, Milwaukee, Wisconsin. Address correspondence and reprint requests to G. Sharat Lin, PhD, Advanced Imaging Associates, Cassio Cir, Fremont, CA Downstream intracranial vascular resistance is routinely evaluated in the carotid arteries by duplex Doppler ultrasonography for quantifying blood flow velocity over a cardiac cycle. Doppler parameters such as pulsatility index (PI), 1 6 resistance index (RI), 6,7 systolic-diastolic ratio (S/D), 8 and diastolic volume index 9 have been used to classify the severity of occlusive disease, to plan treatment, and to monitor response to therapy. The accuracy of these measures of vascular resistance and avoidance of the possible sources of variability are, therefore, of crucial clinical importance. The variability in reading spectral Doppler blood flow velocities at or around the carotid bifurcation is widely recognized and appears to be due less to interobserver or intraobserver variability than to the variability of the spectral waveforms themselves Poor spectral reproducibility has been attributed to disturbed flow patterns 2001 by the American Institute of Ultrasound in Medicine J Ultrasound Med 20: , /01/$3.50

2 Doppler Flow Index Evaluation at the Carotid Bifurcation even in healthy subjects, 12 normal anatomic variations, 13 and varying distances between the Doppler sampling point in the common carotid artery (CCA) and the bifurcation, 14 yet little attempt has been made to visualize the spatial patterns of Doppler indices. The spatial variation of Doppler indices, particularly PI, was studied with hemodynamic color Doppler imaging (HCDI), a novel method of mapping color Doppler indices instead of ultrasonic frequency shifts. The dimensionless ratios make the color mapping relatively independent of Doppler angle. Hemodynamic color Doppler imaging has been shown to be useful in visualizing both intervessel and intravascular variation of pulsatility and vascular resistance. 15 The purpose of this study was to use HCDI to observe how these indices are altered by flow patterns at the bifurcation and the distance upstream over which they are affected. Also of interest was how the CCA waveform transitions to the very divergent pulsatility characteristics of the internal carotid artery (ICA) and external carotid artery (ECA). Understanding how, when, and where Doppler indices are affected by the carotid bifurcation may enable formulation of guidelines for taking more accurate Doppler measurements. Materials and Methods Hemodynamic color Doppler imaging produces a two-dimensional image of color-coded PI, RI, and S/D values superimposed on a B-scan image. This imaging method is based on conventional color Doppler imaging (CDI), in which mean frequency shifts are estimated for each pixel in a color region of interest. By recording 2 or more complete cardiac cycles, relative estimates of peak systolic velocity, end-diastolic velocity, maximum diastolic deflection, and time-averaged mean velocity were obtained at each color pixel. From these, estimated PI, RI, and S/D were computed. Other spectral parameters, such as systolic acceleration slope, could also be mapped but have not yet shown any consistent correlation with hemodynamics or disease. The method and its validation studies have been described previously. 15 Although Doppler indices were estimated by using mean (instead of peak) velocities, the mean velocities of CDI have been shown to provide a realistic quantitative picture of the spatial pattern of blood flow. 16 Although PI, RI, and S/D are conventionally defined in terms of peak velocities or frequency shifts, ratios of means consist of underestimates of peaks in both the numerator and denominator, thus approximately canceling out the underestimates. In any case, HCDI estimates of PI, RI, and S/D were used for visualization of spatial variation and not for point quantification. A Gateway ultrasonographic scanner (GE Diasonics, Santa Clara, CA) was modified with HCDI software to compute the various Doppler indices from mean frequency shifts over 32 successive CDI frames at each color pixel. If, after high-pass filtering, at least half of the CDI frames had no displayed color data at a given pixel, frequency shift information was assumed to be insufficient to properly estimate a Doppler index, and no color was displayed at that pixel in HCDI. The PI was computed according to the method of Gosling and King 2 : where v PS was the blood flow velocity at peak systole, v MD was the blood flow velocity at maximum diastolic deflection, and v was the velocity time averaged over the cardiac cycle. The RI was calculated by the formula of Planiot et al 7 : where v ED was the blood flow velocity at enddiastole. In HCDI, PI, RI, and S/D were actually computed from mean frequency shifts in CDI, which were not corrected for Doppler angle. Doppler index values from low to high were mapped into a rainbow (blue-green-yelloworange-red) color scale for superposition over the two-dimensional gray scale B-scan image. Survey scanning was done in CDI to check for aliasing and to adjust the color pulse repetition frequency before actually acquiring data. The resulting pulse repetition frequencies were set in the range of 3 to 4 khz. To increase the probability of sampling the very transient systolic peak, the CDI frame rate was maximized by limiting the width and depth of the CDI region of interest. Color Doppler imaging frame rates of 11 to 18 frames per second were maintained, yielding a minimum of 12 frames per cardiac cycle. At the minimum frame rate of 11 frames per second, it was possible that a narrow systolic peak could be 1330 J Ultrasound Med 20: , 2001

3 Lin et al missed and quite probable that the true peak (of the mean velocity) might have been underestimated. However, with 32 frames, it was generally possible to average data points over 2 cardiac cycles to obtain more stable Doppler index values. Because PI, RI, and S/D are ratios, the result is a ratio of probable underestimates, and the HCDI color mapping is a qualitative representation of relative values. In practice, HCDI images were found to be highly reproducible. Twenty carotid artery bifurcations were examined in 10 healthy volunteers (7 male and 3 female, age range, 5 75 years) with a 12-MHz linear array operating at 6-MHz color and spectral Doppler settings. Informed consent was obtained from all subjects after the nature of the procedures had been fully explained. Both transverse (cross-sectional) and longitudinal views of the carotid arteries were acquired. The transverse views were obtained by angling the transducer slightly, about 15 to 20 from perpendicular in the elevational plane, to provide a usable Doppler angle of 70 to 75. Because of the angle independence of ratios, variations in transducer inclination had little impact on the color mapping of PI, RI, and S/D. The high-pass wall filter setting was reduced to 25 Hz to ensure detection of smaller frequency shifts at these Doppler angles and to reduce dropout in HCDI color mapping. Transverse cross-sectional views were taken at 1-cm intervals from 5 cm proximal to +1 cm distal to the bifurcation flow divider. Longitudinal views were taken through the carotid bulb on the ECA side of the CCA, including the ECA within the imaging plane where possible. Another view on the ICA side of the CCA was taken to include the ICA wherever it lay in the same plane. Such views were used to visualize transitions in Doppler indices as blood moved from the CCA into its branches. The spatial patterns of PI, RI, and S/D seen on HCDI were checked against spectral Doppler measurements of these indices at the origins of the ECA and ICA and at various distances proximal to the bifurcation flow divider. The overall geometry of the carotid bulb was characterized by-defining the diameter expansion gradient ( d ) as follows: where d BA was the vascular diameter at the bulb apex, d CCA was the vascular diameter in the proximal CCA, and l CCA-BA was the longitudinal distance from the proximal beginning of the bulb (where diameter expansion begins, as shown by cross-sectional CDI) to the bulb apex. All diameters were measured along the ICA-ECA axis. Results Although CDI showed Doppler frequency shifts that were related to mean blood flow velocities, it provided little hint of the hemodynamic differences between the ECA and ICA in disease-free carotid arteries. In Figure 1A, transverse crosssectional CDI shows no difference in core flow velocity between the ECA and ICA at the bifurcation flow divider. In Figure 1B, HCDI of the identical location clearly shows a notable difference in core flow PI between the ECA and ICA. In our series of healthy subjects, the spectral Doppler PIs (mean ± SD) were 1.8 ± 0.25 and 1.3 ± 0.17 at the origins of the ECA and ICA, respectively. In Figure 1A, CDI poorly shows higher velocities in the vessel cores versus lower velocities at the vessel walls. By contrast, in Figure 1B, HCDI shows the elevation of PI in peripheral blood flow in the ICA, which had been previously attributed to increased flow resistance and boundary layer phenomena at the vessel walls. 15,17 Peripheral elevation of PI was also present in the ECA but could not be shown by this particular color mapping, because both core and peripheral flow PIs were above the threshold for the highest colorrendering category (red). Spectral Doppler imaging confirmed a 35% to 45% increase in PI at the vessel walls over core flow in the ICA and a 15% to 20% increase in the ECA. Transverse HCDI images taken at 1-cm intervals upstream from the carotid bifurcation flow divider are shown in Figure 1, C, F, and H. At each level, low-resistance core flow was seen only on the ICA side of the CCA. The ECA side consistently showed higher PI than the ICA side throughout the first 5 cm upstream from the bifurcation flow divider. The spectral Doppler RI in the CCA at 3 cm upstream from the flow divider measured 0.65 at the proximal wall, 0.47 on the ECA side of core flow, 0.56 on the ICA side of core flow, and 0.66 at the distal wall. This confirmed both the eccentric distribution of upstream pulsatility in core flow and the elevation of pulsatility due to increased resistance to J Ultrasound Med 20: ,

4 Doppler Flow Index Evaluation at the Carotid Bifurcation pulsatile flow at the vessel walls. As shown in Figure 1G, CDI at 5 cm upstream still failed to detect this hemodynamic eccentricity. Longitudinal views through the carotid bulb were consistent with what was seen in transverse cross sections. Images in Figure 2, A and B, were taken on the ECA side of the carotid bulb (cut plane L E in Fig. 6A) and include short segments of the ECA and ECA side of the CCA. Hemodynamic color Doppler imaging showed continuity of high PI throughout that side of the carotid bulb. Images in Figure 2, C and D, were taken on the ICA side of the carotid bulb (cut plane L I in Fig. 6A) at CDI and HCDI control settings identical to those of Figure 2, A and B. HCDI displayed continuity of low PI from the ICA side of the CCA through the carotid bulb to the ICA itself. No turbulence or reverse flows could be detected in this case. Upstream laminar flow partitioning between ECA and ICA flows based on Doppler indices was reliably shown in the first 5 cm proximal to the bifurcation flow divider and beyond. Figures 3 and 4 show a healthy left carotid artery with evidence of normal reverse flow at the periphery of the carotid bulb. All CDI images (Figs. 3, A and C, and 4, A and C) show peripheral reverse flows, most likely due to abrupt expansion of a cross-sectional area from the CCA into the carotid bulb. Because the observed reverse flows were localized and coherent, they were not indicative of turbulence. The oblique orientation of some reverse flows (Fig. 4, A and C) suggested a helical twist, as in vortex flow. At the level of the bifurcation flow divider (Fig. 3B) and in the carotid bulb (Fig. 3D), HCDI showed a low PI on the ICA side, a higher PI on the ECA side, and an aberrant (apparently low) PI in the larger reverse flow. Spectral Doppler imaging suggested that this low PI reading (0.80) may Figure 1. Transverse cross sections of the right CCA and jugular vein of a healthy subject. A, Color Doppler image at the carotid bifurcation flow divider showing origins of the ECA (left) and ICA (right) with no color differentiation and no evidence of reverse flow, vortex flow, or turbulence. B, Hemodynamic color Doppler image of PI at the same level showing clear differentiation between high PI (red) at the origin of the ECA versus low PI (green) in core flow at the origin of the ICA. C, Hemodynamic color Doppler image at 1 cm proximal to the bifurcation flow divider showing such high pulsatility on the ECA side that PI cannot be calculated because of diastolic color dropout. The ICA side continues to show low PI in core flow. D, Hemodynamic color Doppler image at 2 cm proximal showing an eccentric location of low-pi core flow favoring the ICA side. E, Hemodynamic color Doppler image at 3 cm. F, Hemodynamic color Doppler image at 4 cm. G, Color Doppler image at 5 cm proximal, which fails to show hemodynamic eccentricity. H, Hemodynamic color Doppler image at the same level, which continues to show laminar flow partitioning between the impending ECA and ICA flows. A B C D E F G H 1332 J Ultrasound Med 20: , 2001

5 Lin et al have been depressed because of the absence of a very short interval of forward or reverse flow, because the flow was, in fact, bidirectional, as indicated by its bipolar waveform (Fig. 5). The bidirectional flows at opposite walls of the carotid bulb had no frequency shift at end diastole, yielding spectral Doppler RIs of 1.0. The same pattern was observed by HCDI for RI and S/D (Fig. 3, E and F), including elevation of Doppler indices at the vessel walls. However, upstream from the reverse flow at 2 and 3 cm (Fig. 3, G and H), the core flow was symmetrically distributed, with no observable distinction between ECA and ICA sides. For example, in the case depicted in Figures 3 and 4, the spectral Doppler RI in core flow on the ECA side of the bulb and proximal CCA (mean ± SD) was 0.71 ± 0.9 versus 0.69 ± 0.4 on the ICA side. Figure 2. Longitudinal views of the right carotid and jugular vein of Figure 1. A, Color Doppler image of the ECA (left) and ECA side of the CCA (right). B, Same view with HCDI showing consistently high-pi flow throughout. C, Color Doppler image of the ICA (left) and ICA side of the CCA (right). D, Hemodynamic color Doppler view of C showing consistently low-pi core flow throughout. A B C D J Ultrasound Med 20: ,

6 Doppler Flow Index Evaluation at the Carotid Bifurcation Perhaps the most direct evidence of obliteration of the respective pulsatility characteristics of ECA and ICA flows by reverse and vortex flows in the carotid bulb is shown by HCDI in longitudinal sections in Figure 4, B and D (corresponding to cut planes L E and L I, respectively, in Fig. 6B). Here, an oblique belt of reverse flow forms the precise boundary between high-pi ECA and moderate-pi CCA flow characteristics and between low-pi ICA flow characteristics and CCA flow. Of the 20 carotid arteries examined, 15 had normal reverse or vortex flow at the carotid bulb, which caused mixing of blood flows, locally obliterating laminar flows and abolishing upstream laminar flow partitioning. Under these conditions, the CCA exhibited pulsatility characteristics that were a composite of the ECA and ICA, and its core flow was approximately radially symmetrically distributed. These findings on CDI and HCDI were confirmed by spectral Doppler measurements (Table 1). There was no significant difference between core flow PI on the ICA side versus the ECA side at 2 to 4 cm upstream in the CCA (P >.2). Conversely, in the absence of detectable reverse or vortex flow in the carotid bulb, upstream laminar flow partitioning was sustained to at least 5 cm proximal to the bifurcation flow divider. The difference between core flow PI on the ICA side versus the ECA side in the CCA was statistically significant (P <.007). Only 5 of 20 carotid arteries had no evidence of reverse or vortex flow. The absence of detectable reverse flow was correlated with laminar flow streaming through the carotid bulb into the ICA and ECA, resulting in upstream flow partitioning into parallel low- and high-resistance (pulsatility) streams in the CCA shown in Figure 6A. This may occur when the expansion of the vascular cross section from the CCA to the bulb is comparatively moderate and gradual. In the carotid artery shown in Figure 1, Figure 3. Transverse cross-sections of the left CCA of a healthy subject. A, Color Doppler image at the carotid bifurcation flow divider showing origins of ECA (left) and ICA (right) with no color differentiation but with evidence of peripheral reverse flow (blue). B, Hemodynamic color Doppler image of PI at the same level showing clear differentiation between high PI (red) on the ECA side and low PI (green) in core flow on the ICA side. C, Color Doppler image at 1 cm proximal to the bifurcation flow divider showing substantial normal vortex flow (peripheral reverse flows in blue). D, Hemodynamic color Doppler image at 1 cm proximal showing low PI on the ICA side (right) and in reverse flow (top left). E, Hemodynamic color Doppler image of RI at 1 cm showing a similar pattern. F, Hemodynamic color Doppler image of S/D at the same level. G, Hemodynamic color Doppler image at 2 cm showing symmetric low-pi core flow. H, Hemodynamic color Doppler image at 3 cm. A B C D E F G H 1334 J Ultrasound Med 20: , 2001

7 Lin et al the expansion of the vascular diameter along the ICA-ECA axis was approximately 57% (from 7 mm in the CCA to 11 mm at the bifurcation flow divider) over a length of 4 cm along the vessel (Fig. 1, from F to B). The diameter expansion gradient was 0.1. Reverse and vortex flows, helical patterns usually seen as oblique segments of reverse flow, disrupt laminar streams and are associated with flow mixing in the carotid bulb. They obliterate upstream laminar flow partitioning, resulting in a relatively symmetric transverse flow profile across the proximal CCA, as shown in Figure 6B. This may happen when the expansion in the vascular cross section from the CCA to the bulb is comparatively large and steep. In the carotid Figure 4. Longitudinal views of the left carotid artery of Figure 3. A, Color Doppler image of the ECA (left) and ECA side of the CCA (right) showing reverse flows (blue). B, Same view on HCDI showing an abrupt transition between high-pi ECA and medium-pi CCA. C, Color Doppler image of the ICA (left) and ICA side of the CCA (right), also showing peripheral reverse flow. D, Hemodynamic color Doppler view of C showing how reverse flow of the vortex marks a precise transition between low-pi ICA and medium-pi CCA. Note how the HCDI color rendering of the CCA is virtually the same on both the ECA and ICA sides. A B C D J Ultrasound Med 20: ,

8 Doppler Flow Index Evaluation at the Carotid Bifurcation Figure 5. Triplex color Doppler image of the left carotid bulb of Figure 3. The oblique reverse flow pattern suggests a vortex. Spectral Doppler imaging confirms decisive reverse flow at mid-diastole and extremely high calculated PI. artery shown in Figure 3, the expansion of vascular diameter along the ICA-ECA axis was approximately 87% (from 8 mm in the CCA to 15 mm at the bifurcation flow divider) over a length of 2 cm along the vessel (Fig. 3, from E to B). This resulted in a diameter expansion gradient of The 5 carotid arteries with no detectable reverse or vortex flows had a diameter expansion gradient (mean ± SD) of 0.13 ± 0.03 versus the 15 carotid arteries exhibiting reverse or vortex flow with a diameter expansion gradient of 0.22 ± 0.06 (P <.05). This suggests that the shape of the carotid bulb itself may be the primary determinant of upstream flow characteristics. Abrupt expansion of the vascular diameter gives rise to reverse and vortex flows as forward-moving blood rushes toward the walls to fill voids in the expanding vascular cross section and backward along the walls to pockets of low pressure. This is consistent with the results of previous authors indicating that reverse flows are concentrated at the ends of the major diameter of the bulb (the ICA-ECA axis) and longitudinally along the opposite outer walls of the proximal ICA and ECA When the bulb is long and widens more gradually, this occurs less frequently. Velocity adjustments alone are sufficient to compensate for the more gradual change in vessel cross-sectional area to maintain a constant volume flow throughout the carotid artery and consequently preserving laminar flow. This is corroborated by the results of fluid dynamic modeling in which smooth, gradually tapered carotid bifurcation geometry (no bulb) resulted in minimal wall shear stress gradients. 19 Our results confirm that this principle also applies to the presence or absence of reverse flows in vivo. From the case shown in Figure 1, PI estimates across a diameter of the CCA were tabulated from histograms obtained along the transverse ECA-ICA axis in HCDI images. Two sequences of histograms were acquired at 0.5-cm intervals proximal to the bifurcation flow divider, where each diameter histogram was sampled at 16 equally spaced data points. Thus, the spacing between cross-sectional data points was not a Figure 6. Schematic diagrams of carotid bifurcation and CCA showing 7 planes of transverse imaging and 2 planes of longitudinal imaging (L E going through the ECA side of the carotid bulb and L I cutting through the ICA side). A, Upstream laminar flow partitioning associated with the absence of detectable reverse or vortex flow in a minimal carotid bulb. B, Mixed upstream pulsatility characteristics associated with reverse and vortex flows in a typical carotid bulb. A B 1336 J Ultrasound Med 20: , 2001

9 Lin et al Table 1. Spectral Doppler Measurements of PI in Core Flow for 20 Carotid Arteries Categorized According to the Presence or Absence on CDI of Reverse or Vortex Flow in the Carotid Bulb Flow PI in ECA core PI in ICA core PI in CCA core, ECA side PI in CCA core, ICA side P* Reverse (n = 15) 1.71 ± ± ± ± No reverse (n = 5) 1.93 ± ± ± ± Values are mean ± SD. *Difference between ECA versus ICA side. fixed distance interval but instead depended on the diameter of the CCA at the location sampled. The actual diameter varied from 7 mm in the proximal CCA to 11 mm in the carotid bulb. The PI values from the 2 sets of HCDI histograms were averaged together and plotted in Figure 7A, which graphically shows sustained upstream laminar flow partitioning in a CCA in the absence of detectable reverse flow or turbulence. However, it also shows the incremental equalization of core flow PI between ECA and ICA sides. Most importantly, as a potential source of measurement error, PI varied by up to ±30% on either side of the mean for core flow, depending of the location of spectral Doppler sampling on the ECA side or the ICA side. With the use of the same method for the carotid artery shown in Figure 3, PI values from 2 sets of histograms were averaged together and plotted in Figure 7B. The actual diameter varied from 8 mm in the proximal CCA to 15 mm in the carotid bulb. In this case, with peripheral reverse flows in both the ECA and ICA sides of the carotid bulb, high computed PI estimates were due to reading of bidirectional flows at the vessel walls. However, immediately proximal to the reverse flows was a region of relative symmetry in the transverse PI profile. This further illustrates the notion that reverse flow, vortex flow, or turbulence causes mixing in the carotid bulb, which obliterates upstream partitioning between ECA and ICA flow characteristics. Discussion The carotid bifurcation presents a particular challenge because of its complex luminal topography The morphology of the carotid bulb and its bifurcation angle are extremely varied, contributing to often-unanticipated variability of flow patterns, which may contribute to inaccurate measurements of velocity, PI, RI, and S/D. Figure 7. Transverse PI profile across diameters of CCAs in the first 5 cm proximal to the bifurcation flow divider. For graphing purposes, carotid diameters were normalized by taking 16 equally spaced samples from wall to wall. A, Common carotid artery with no detectable reverse or vortex flow in the carotid bulb. Actual diameters varied from 7 mm in the proximal CCA to 11 mm at the flow divider. The ECA and ICA sides retained their respective pulsatility signatures even at 5 cm proximal. B, Common carotid artery with peripheral vortex flow in the carotid bulb. Actual diameters varied from 8 mm in the proximal CCA to 15 mm at the flow divider. The PI profile became symmetric immediately upstream from the vortex flows at approximately 2 cm proximal to the bifurcation flow divider. A B J Ultrasound Med 20: ,

10 Doppler Flow Index Evaluation at the Carotid Bifurcation The cross-sectional area of the CCA widens into the carotid bulb, causing reverse flows at the vascular walls. This gives rise to a normal tendency for either linear reverse flow or vortex flow (seen in CDI as segments of coherent reverse flow). Such zones of flow reversal may extend into the proximal ends of the ICA and ECA. 18,25 Reverse and vortex flows disrupt laminar flows, thus abolishing upstream laminar flow partitioning in the CCA. The presence of reverse and vortex flows does not necessarily indicate stenosis but has been routinely observed in healthy carotid arteries. A combination of in vivo studies, in vitro models, and theoretical modeling of fluid dynamics indicates that reverse and vortex flows are a result of the inherent geometry of the normal carotid bifurcation. 18,22,23,26 29 On the other hand, reverse flows occur where atherosclerotic plaque commonly develops, suggesting that reverse flow may play a role in plaque pathogenesis. 18,20 29 The results of our study suggest that measurement of flow velocity and Doppler indices in the CCA just proximal to the bifurcation is likely to be very location sensitive. The thickness of circumferential boundary layers with elevated PI, RI, and S/D and restricted flow velocities should be an important consideration in deciding where to position a spectral Doppler sample volume. The elevation of PI, RI, and S/D at carotid artery walls correlates well with calculated wall shear stress across the vessel. 17,19 When reverse or vortex flows are present in the carotid bulb, measurement of Doppler indices in the CCA requires positioning of a small sample volume in the center of the lumen at least 3 cm proximal to the flow divider. However, in the absence of such reverse or vortex flows, the Doppler sample volume should be positioned as far upstream as possible. Although somewhat time-consuming, taking several measurements at different locations both laterally and axially in the CCA can provide reasonable assurance of stable core flow if the measurements are relatively consistent. Highly variable results in core flow would suggest that upstream laminar flow partitioning is present and that measurements must be taken farther upstream or that multiple measurements must be averaged together to obtain a representative reading. Although CDI is useful in visualizing flow boundaries and in detecting flow reversal, vortices, and turbulence, it does not provide useful information on functional hemodynamics, including pulsatility and laminar flow effects. Hemodynamic color Doppler imaging can be an effective tool for reproducibly visualizing spatial patterns of Doppler indices and guiding placement of a spectral Doppler sample volume within stable core flow to increase confidence in the accuracy and reproducibility of measurements. References 1. Cooperberg E. Ultrasound Doppler spectral analysis in the diagnosis of occlusive lesions of the carotid arteries. Ultrasound Med Biol 1992; 18: Gosling RC, King DH. Arterial assessment by Doppler shift ultrasound. Proc R Soc Med 1974; 67: Jackson S, Vyas S. A double-blind, placebo controlled study of postmenopausal oestrogen replacement therapy and carotid artery pulsatility index. Br J Obstet Gynaecol 1998; 105: Urabe T, Shioya-Morikawa N. Differentiation of embolic and thrombotic middle cerebral artery occlusion using ultrasonic carotid flow velocity analysis. J Neurol Sci 1995; 128: Blohme L, Pagani M, Parra-Hoyos H, Olofsson P, Takolander R, Swedenborg J. Changes in middle cerebral artery flow velocity and pulsatility index after carotid endarterectomy. Eur J Vasc Surg 1991; 5: Whyman MR, Naylor AR, Ruckley CV, Wildsmith JAW. Extracranial carotid artery flow measurement during carotid endarterectomy using a Doppler ultrasonographic flowmeter. Br J Surg 1994; 81: Planiot T, Pourcelot L, Pottier J-M, Degiovanni E. Étude de la circulation carotidienne par les méthodes ultrasoniques et la thermographie. Rev Neurol (Paris) 1972; 126: Archie JP. A simple, non-dimensional, normalized common carotid Doppler velocity wave-form index that identifies patients with carotid stenosis. Stroke 1981; 12: Weskott HP, Holsing K. US-based evaluation of hemodynamic parameters in the common carotid 1338 J Ultrasound Med 20: , 2001

11 Lin et al artery: a nomogram trial. Radiology 1997; 205: Polak J, Dobkin G, O Leary D, Weng A, Cutler S. Internal carotid artery stenosis: accuracy and reproducibility of color Doppler-assisted duplex imaging. Radiology 1989; 173: Mikkonen RHM, Kreula JM, Virkkunen PJ. Reproducibility of Doppler ultrasound measurements. Acta Radiol 1996; 37: Kohler T, Langlois Y, Roederer GO, et al. Sources of variability in carotid duplex examination: a prospective study. Ultrasound Med Biol 1985; 11: Prendes JL, McKinney WM, Buonanno FS, Jones AM. Anatomic variations of the carotid bifurcation affecting Doppler scan interpretation. J Clin Ultrasound 1980; 8: Meyer JI, Khalil RM, Obuchowski NA, Baus LK. Common carotid artery: variability of Doppler US velocity measurements. Radiology 1997; 204: Lin GS, Spratt RS. Hemodynamic imaging with pulsatility-index and resistance-index color Doppler US. Radiology 1997; 204: Branas CC, Weingarten MS, Czeredarczuk M, Schafer PF. Examination of carotid arteries with quantitative color Doppler flow imaging. J Ultrasound Med 1994; 13: Samijo SK, Willigers JM, Brands PJ, et al. Reproducibility of shear rate and shear stress: assessment by means of ultrasound in the common carotid artery of young human males and females. Ultrasound Med Biol 1997; 23: Polak JF. Doppler sonography: an overview. In: Peripheral Vascular Sonography: A Practical Guide. Baltimore, MD: Williams & Wilkins; 1992: Wells DR, Archie JP Jr, Kleinstreuer C. Effect of carotid artery geometry on the magnitude and distribution of wall shear stress gradients. J Vasc Surg 1996; 23: in a human carottid bifurcation: a combined CFD and MRI study. J Magn Reson Imaging 2000; 11: Phillips DJ, Greene FM Jr, Langlois Y, Roederer GO, Strandness DE Jr. Flow velocity patterns in the carotid bifurcations of young, presumed normal subjects. Ultrasound Med Biol 1983; 9: Zierler RE, Phillips DJ, Beach KW, Primozich JF, Strandness DE Jr. Noninvasive assessment of normal carotid bifurcation hemodynamics with color-flow ultrasound imaging. Ultrasound Med Biol 1987; 13: de Bray JM, Galland F, Lhoste P, et al. Color Doppler and duplex sonography and angiography of the carotid artery bifurcations. Neuroradiology 1995; 37: Ku DN, Giddens DP, Phillips DJ, Strandness DE Jr. Hemodynamics of the normal human carotid bifurcation: in vitro and in vivo studies. Ultrasound Med Biol 1985; 11: Middleton WD, Foley WD, Lawson TL. Flow reversal in the normal carotid bifurcation: color Doppler flow imaging analysis. Radiology 1988; 167: Strandness DE Jr. Hemodynamics of the normal arterial and venous system. In: Duplex Scanning in Vascular Disorders. 2nd ed. New York, NY: Raven Press; 1993: Fukushima T, Homma T, Harakawa K, Sakata N, Azuma T. Vortex generation in pulsatile flow through arterial bifurcation models including the human carotid artery. J Biomech Eng 1988; 110: Schuierer G, Huk WJ. Diagnostic significance of flow separation within the carotid bifurcation demonstrated by digital subtraction angiography. Stroke 1990; 21: Polak JF, O Leary DH, Quist WC, Creager MA, LoGerfo FW. Pulsed and color Doppler analysis of normal carotid bifurcation flow dynamics using an in-vitro model. Angiology 1990; 41: Long Q, Xu XY, Ariff B, Thom SA, Hughes AD, Stanton AV. Reconstruction of blood flow patterns J Ultrasound Med 20: ,

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