Opinion. Technical aspects of aortic isthmus Doppler velocimetry in human fetuses

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1 Ultrasound Obstet Gynecol 2009; 33: Published online in Wiley InterScience ( DOI: /uog.6406 Opinion Technical aspects of aortic isthmus Doppler velocimetry in human fetuses The aortic isthmus is the segment of aorta located between the origin of the left subclavian artery and the connection of the ductus arteriosus to the descending aorta. In the postnatal period following the closure of the ductus arteriosus, it serves only as a vascular conduit transporting blood from the aortic arch down to the descending aorta. However, during prenatal life, it plays an important role in maintaining an adequate balance between the brachiocephalic circulation supplying the upper body (including the brain) and the subdiaphragmatic circulation supplying the lower body and placenta 1. The parallel arrangement of the fetal circulation allows for unequal right and left ventricular outputs as the placental, pulmonary and lower body vascular resistances act mainly on the right ventricle, whereas the upper body resistance acts mainly on the left ventricle 2. Under physiological conditions and in the absence of structural cardiovascular malformations, such as hypoplastic left heart syndrome, critical aortic stenosis and interrupted aortic arch, the flow in the aortic isthmus is forward during the whole cardiac cycle. The volume and direction of aortic isthmus blood flow are determined by the systolic performance of the individual ventricles and the peripheral vascular resistances. During systole, the left ventricular ejection facilitates forward flow while the right ventricular ejection has the opposite effect. During diastole, when the ventricles are not ejecting blood and both semilunar valves are closed, the direction of blood flow in the aortic isthmus depends mainly on the relative difference between the upper body (including brain) and lower body (including placenta) vascular resistances 1. Therefore, conditions that lead to an increased right ventricular afterload (e.g. intrauterine fetal growth restriction due to placental insufficiency) or a reduced left ventricular afterload (e.g. hypoxemia, cerebrovascular aneurysms, vascular tumors of the neck) may cause a reversal of aortic isthmus blood flow during diastole. Several experimental studies on sheep fetuses 3 6 have established the pathophysiological basis for using aortic isthmus Doppler velocimetry in the evaluation of fetal cardiovascular dynamics. Furthermore, clinical studies have shown the feasibility of recording aortic isthmus blood flow velocity waveform in the human fetus 7 10, and abnormal blood flow pattern has been shown to be associated with fetal circulatory redistribution or compromise Recently, aortic isthmus Doppler velocimetry has been shown to predict perinatal 16 and long-term neurodevelopmental 17 outcomes in placental insufficiency and the routine use of aortic isthmus Doppler velocimetry has been suggested in the evaluation of fetuses with intrauterine growth restriction 18. Obviously, some centers with expertise make use of aortic isthmus Doppler velocimetry in addition to other arterial and venous Doppler parameters in the investigation of fetal hemodynamics, but the perceived technical difficulties have led to some skepticism regarding its potential for wider clinical application. A multicenter study on the feasibility and reliability of aortic isthmus Doppler velocimetry published in this issue of Ultrasound in Obstetrics and Gynecology 19 showed that, despite adequate visualization and accurate identification of this vascular segment, appropriate cursor placement for pulsed-wave Doppler interrogation of aortic isthmus blood flow velocity waveforms remains challenging. The purpose of this article is to give some practical advice to clinicians on how to perform aortic isthmus Doppler blood flow velocimetry in the human fetus. Today, with improved ultrasound imaging technology, appropriately trained obstetricians and fetal/perinatal cardiologists obtain standard views of the fetal heart and great vessels without much difficulty. The aortic isthmus can be identified easily in both the longitudinal (Figure 1a c) and cross-sectional (Figure 1d) views that are used routinely during fetal echocardiography. Once this vascular segment is identified, Doppler velocimetry can be performed in any of the views shown in Figure 1 by placing the Doppler gate (cursor) at the appropriate location, keeping the angle of insonation as low as possible. Although Doppler flow velocity waveforms can be obtained using B-mode imaging and pulsed-wave Doppler (Figure 1c), color-directed pulsed-wave Doppler interrogation is recommended, as it helps in the identification of the vessels and shows the direction of the blood flow, allowing optimal positioning of the cursor. Pulsed-wave gate size (sample volume) should be adjusted according to the size of the aortic isthmus, which depends on the fetal gestational age, to avoid recording signals from the adjacent vessels. Blood flow velocity waveforms are recorded during fetal quiescence. The aortic isthmus flow velocity waveforms obtained from either of the sonographic planes (longitudinal aortic arch view or three vessels and trachea view) are quite similar (Figure 2) and reproducible 9,20. Accurate cursor positioning may be simpler in the longitudinal view, as the origin of the left subclavian artery is relatively easier to visualize in this plane and there is less possibility of obtaining blood flow velocity waveforms from the transverse aortic arch rather than the isthmus. On the other hand, it may be simpler, easier and less time-consuming Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd. OPINION

2 Opinion 629 Figure 1 Longitudinal (a c) and cross-sectional (d) imaging planes demonstrating the aortic isthmus with correct cursor placement for pulsed-wave Doppler interrogation. The arrow indicates the left subclavian artery. DA, ductus arteriosus; DAo, descending aorta. to obtain the three vessels and trachea view rather than the longitudinal aortic arch view. The aortic isthmus flow velocity waveform has a typical shape and is easily recognizable in most instances. It has a quick systolic upstroke (short acceleration time), with mean peak systolic velocities ranging between approximately 30 and 100 cm/s from 11 weeks to term 10,21. This is followed by a more gradual deceleration of the velocity and a narrow incisura (in most cases) at the end of systole. A small flow reversal for a very short period of time is usually seen at end-systole (Figure 3a) in the third trimester of pregnancy 7,8. However, this brief endsystolic flow reversal is absent before 20 weeks 7,21 and is recorded less commonly when the aortic isthmus flow velocity waveforms are obtained in the cross-sectional imaging plane (three vessels and trachea view) 10. Reversal of blood flow during diastole or net blood flow reversal (i.e. total retrograde flow > total antegrade flow during the cardiac cycle) in the aortic isthmus (Figure 3b) is always abnormal. As the ductus arteriosus is in close proximity to the aortic isthmus (Figure 1a and d), even very small movements may lead to the waveforms being obtained from one or the other vessel during pulsed-wave Doppler interrogation (Figure 4). Frequently updating the B-mode or the color flow images may be necessary to ensure that the pulsed-wave gate remains in the correct position during acquisition of Doppler flow velocity waveforms. Generally speaking, ductus arteriosus Doppler waveforms differ slightly from those of the aortic isthmus (Figure 5). Gestational-age specific mean peak systolic velocities of the ductus arteriosus are much higher than are those of the aortic isthmus, ranging between 40 and 120 cm/s from 11 weeks to term In fact, the ductus arteriosus has the highest blood flow velocities in the fetal circulation 25. In contrast to the aortic isthmus, the brief reversal of flow at end-systole is usually not seen in the ductus arteriosus and positive diastolic velocities are almost always present under physiological conditions. The forward flow during systole starts and peaks in the aortic isthmus earlier than it does in the ductus arteriosus (Figures 3 and 6). Experimental studies in sheep fetuses have shown that the pre-ejection period of the right ventricle is longer than is that of the left (57 vs. 48 ms) 26, and the ductal flow begins approximately 48 ms later than does the isthmic flow and has a longer acceleration time (52 vs. 18 ms) 27. Occasionally, especially while interrogating using a larger sample volume, one may obtain simultaneously aortic isthmus and ductus arteriosus blood flow velocity waveforms,

3 630 Acharya Figure 2 Doppler flow velocity waveforms obtained from the aortic isthmus using longitudinal (a,b) and cross-sectional (c,d) imaging planes with and without color Doppler. Figure 3 Typical normal (a) and abnormal (b) aortic isthmus Doppler flow velocity waveforms in the third trimester. In (a), the arrow points to the incisura and the arrowhead points to the brief retrograde flow at end-systole. In (b), small arrowheads point to the ductus arteriosus blood flow velocity waveforms in the background. Note that the aortic isthmus flow is reversed in late systole and the whole of diastole (net flow is retrograde). Figure 4 Blood flow velocity recordings from the ductus arteriosus. (a) is a normal waveform; (b) shows that very small drift can lead to recording blood flow velocity waveforms from the aortic isthmus (arrows) and vice versa.

4 Opinion 631 Figure 6 Doppler flow velocity waveforms obtained at the level of the aortic isthmus in the longitudinal aortic arch view (a) and three vessels and trachea view (b) with relatively large sample volumes, demonstrating the isthmic waveforms (traced in red) superimposed on the ductal waveforms. Figure 5 Longitudinal views of the aortic arch (a) with asterisk ( ) indicating the isthmus, and the pulmonary-ductal arch (b) with asterisk ( ) indicating the ductus arteriosus. Their corresponding blood flow velocity waveforms are shown in the lower panels. superimposed on each other (Figure 6), making direct comparison during the cardiac cycle possible in human fetuses. It is possible to estimate the aortic isthmus volume blood flow (Q ai ) non-invasively 21 by measuring its diameter and blood flow velocities: Q ai (in ml/min) = time-averaged maximum velocity (TAMXV, in cm/s) π(diameter/2, in cm) However, due to the limitations and complexity of volume flow measurements, several other indices have been proposed for clinical use. Basically, these indices differ in one principle: some use absolute velocities in their calculation whereas others use the velocity-time integral (VTI). Fouron et al. 7 initially proposed a so-called balance index, i.e. (peak systolic velocity end-diastolic velocity/(antegrade VTI retrograde VTI), which is equivalent to pulsatility index (PI) when absolute velocities are used, as the sum of systolic and diastolic VTI multiplied by the fetal heart rate gives TAMXV and PI = (peak systolic velocity end-diastolic velocity)/tamxv. An isthmic flow index (IFI), i.e. (systolic VTI + diastolic VTI)/systolic VTI, was proposed later 8, but has not gained much popularity among clinicians. The argument for using VTI-related indices rather than velocity-related indices has been the assumption that they provide better information on the volume and direction of blood flow. However, this assumption is not entirely true. For example, TAMXV is likely to reflect the volume blood flow, as it does in other vessels 28,29, and a positive TAMXV (or PI) signifies that the net blood flow during the cardiac cycle is antegrade, while a negative value means that the net flow is retrograde in the same way as does a VTI of antegrade flow/vti of retrograde flow ratio of > 1or< 1. Similarly, PI is also likely to reflect the size of the reverse flow component when present, as TAMXV (which is equivalent to VTI

5 632 Acharya over one cardiac cycle heart rate) is the denominator in the formula used for its calculation. The IFI for aortic isthmus blood flow can be divided in five different types 8 as follows: Type I: IFI > 1, when the flow is antegrade throughout the cardiac cycle; Type II: IFI = 1, when diastolic flow is absent; Type III: IFI = 0 1, when the diastolic flow is reversed but the net flow is still antegrade; Type IV: IFI = 0, when the antegrade and retrograde flows are equal; and Type V: IFI < 0, when the net flow is retrograde. However, what really matters is whether the diastolic blood flow is reversed and whether the net blood flow is retrograde, as these are the signs of compromised fetal hemodynamics. In this context, normal and abnormal waveforms can be identified by simple qualitative (visual) assessment as those showing antegrade diastolic flow (IFI values 1) and those showing retrograde diastolic flow (IFI < 1), respectively. Further classification of waveform patterns using IFI into more types does not seem to improve the predictive value for adverse perinatal outcome 8. Aortic isthmus retrograde diastolic blood flow signifies redistribution of fetal circulation, indicating lower upper body (cerebral) resistance compared with lower body (placental) resistance, whereas the reversal of net blood flow indicates that the fetus has problems maintaining cerebral oxygenation 3. Semiquantitative indices like PI and the resistance index (RI) are known to reflect downstream impedance and are easy to calculate using software packages available with most ultrasound machines. The aortic isthmus PI is increased and absolute velocities (especially the TAMXV) are reduced in intrauterine growth-restricted fetuses, regardless of IFI type 16. Furthermore, absolute velocities are quantitative variables that are used in the calculation of PI and RI as well as of volume blood flow. Therefore, using absolute blood velocities and PI rather than IFI may be simpler and more appropriate in clinical practice. However, it is important to be aware of the fact that the brief reversal of flow during end-systole, which is a normal finding in the third trimester, can give falsely high PI values if one calculates the PI as (maximum velocity minimum velocity)/tamxv rather than as (peak systolic velocity end-diastolic velocity)/tamxv. Changes in the aortic isthmus blood flow velocity waveform are evident earlier than are those in the descending aorta 11, umbilical artery 12 and ductus venosus 15,30.An increase in placental resistance causing a 50% reduction in umbilical blood flow has been shown to be associated with reversed aortic isthmus diastolic blood flow in sheep fetuses, even though the umbilical artery diastolic blood flow remained forward 4. Fetuses with absent/reversed end-diastolic flow in the umbilical artery 12,16,17 or in the ductus venosus 15,16 consistently appear to have retrograde diastolic flow in the aortic isthmus. Aortic isthmus blood flow velocimetry provides important information on fetal cardiovascular function, i.e. individual performance of ventricles, relative changes in upper (including brain) and lower (including placenta) body resistances and fetal oxygenation, and has the potential to become a valuable clinical tool. However, as this segment of the fetal aorta is relatively short and has several other blood vessels in its close proximity, obtaining blood flow velocity waveforms can be technically challenging. For accurate measurement and interpretation of the aortic isthmus blood flow using Doppler ultrasonography, it is important that operators receive adequate training in obtaining the standard longitudinal aortic arch view and three vessels and trachea view, visualizing and recognizing the aortic isthmus in B-mode and the direction of blood flow in color flow mode, appropriate cursor placement, recognition of the waveform patterns of the aortic isthmus as well as other adjacent vessels, and that they have an understanding of factors that may influence the blood flow in this segment of fetal circulation. G. Acharya Department of Obstetrics and Gynecology, Institute of Clinical Medicine, University of Tromsø and University Hospital of Northern Norway, Tromsø, Norway Correspondence. University Hospital of Northern Norway, Post Box 24, N-9038 Tromsø, Norway ( ganesh.acharya@uit.no) REFERENCES 1. Fouron JC. The unrecognized physiological and clinical significance of the fetal aortic isthmus. 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