Pediatr Radiol (2004) 34: 757771 DOI 10.

1007/s00247-004-1228-2

REVIEW

Brian D. Coley

Pediatric applications of abdominal vascular Doppler imaging: Part I

Received: 13 March 2004 Revised: 19 April 2004 Accepted: 3 May 2004 Published online: 27 July 2004 Springer-Verlag 2004

B. D. Coley Columbus Childrens Hospital, 700 Childrens Dr., Columbus, OH 43205, USA E-mail: bcoley@chi.osu.edu Tel.: +1-614-7222359 Fax: +1-614-7222332

Abstract Ultrasound is a remarkably powerful and versatile modality for pediatric imaging, without requiring exposure to radiation or sedatives. By providing information on blood ow, Doppler sonography can reveal details about normal physiology and disease processes not discernable from gray-scale anatomic images alone. However, in routine practice in many institutions Doppler remains underutilized, in part due to uncertainty of the

meaning of changes in Doppler waveforms. In part I of this review, the basics of hemodynamics and how changes in blood ow aect the Doppler waveform are reviewed. Clinical applications in the investigation of hepatic disease are then discussed.

Keywords Physics Liver Doppler Ultrasound

Introduction
The utility of US in pediatric diagnosis is well recognized. Unfortunately, with most attention in the literature focusing on advances in CT and MRI, US is sometimes viewed as a less useful modality. While CT and MRI may in some cases provide superior anatomic information, the utility of color and pulsed Doppler US in the evaluation and quantitation of blood ow is dicult to match. This paper will review the basics of hemodynamics, the measurements used to describe them, the causes of blood ow alterations, and the clinical applications of Doppler US in the pediatric abdomen.

Hemodynamics
To better appreciate and interpret Doppler waveforms obtained during clinical examinations, one should have at least a passing understanding of how blood ow contributes to the images. The hemodynamics of steady

ow in a rigid tube are relatively uncomplicated. The eects of pulsatile ow, elastic vessels, curves and bifurcations, and variability of downstream impedance all serve to complicate the hemodynamics of in vivo ow. Nonetheless, by understanding a few basic principles, a practical understanding of ow dynamics can be achieved that will improve appreciation for Doppler information. For those interested in a more detailed discussion than the simplied version presented here, I recommend the highly readable work of Peter Burns [1] and others [24]. When we interrogate a vessel with pulsed Doppler (or color Doppler), what we see displayed on the US screen is a graph of the velocities (y axis) of the blood owing between our sampling gate plotted over time (x axis). The velocity is determined by the Doppler eect and calculated by the formula: FD = 2 F0 v cosh/c In clinical practice, the speed of sound through tissue (c) is presumed to be 1,540 m/s, F0 is the frequency of insonation, the Doppler frequency shift (FD) is measured, and the angle of insonation (h) is determined from the gray-scale image. This allows calculation of the

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single remaining variable (v), the velocity of the blood within the vessel. Flow within most normal vessels is usually regarded as laminar. The viscous properties of blood dictate that the larger the velocity, the greater the shear stress or force of opposition there will be to blood ow. At steady ow rates, this produces laminar ow with a parabolic velocity prole. Blood at the edges of the vessel has essentially no forward velocity (the boundary layer), whereas blood at the center of the vessel has the highest velocity (with the mean velocity equal to one-half of the maximum). In practice, a narrow gate placed within a vessel with parabolic laminar ow will demonstrate a tight velocity prole, whereas a gate encompassing the entire vessel width will show ll-in of the waveform, reecting the inclusion of lower velocity regions of ow in the Doppler signal (Fig. 1). In larger vessels such as the aorta, inertial forces due to rapid acceleration lead to a blunted or plug-shaped ow prole, where velocities are nearly equally distributed across the vessel (with mean velocity approximately equal to the velocity maximum). In practice, the Doppler waveform obtained with either a narrow or wide gate will be essentially the same, reecting the uniformity of the velocity prole (Fig. 2). With pulsatile ow, these velocity proles actually change dramatically during the cardiac cycle [5]. Additionally, ow around a curve shifts the velocity prole, with higher velocities present on the outside of the curve and lower velocities on the inside [1]. Reversed ow or eddy currents can be seen at vessel origins (entrance eect, such as at the profunda femoral artery origin), or at areas of vessel widening (exit eect, such as at the carotid bulb) due to boundary layer separation eects. With laminar ow, ow rate increases linearly with increasing pressure. However, with increasing ow rates, a point will occur where increasingly greater pressures

Fig. 2 Plug ow. The velocities in plug ow are more uniform, so the waveforms obtained with a narrow or wide Doppler gate are nearly identical

are needed to achieve the same increase in ow (Fig. 3). This is the point where turbulent ow occurs, when uniform forward motion within the vessel is disturbed. The point at which ow becomes turbulent is expressed by the Reynolds number for a uid: R = dvp/n, where d = vessel diameter, v = velocity, p = uid mass density, and n = uid viscosity. For blood, a Reynolds number of around 2,000 produces turbulent ow, but this can vary considerably in vivo and even vary during the cardiac cycle [1]. Turbulent ow may be seen as spectral broadening and evidence of bidirectional ow on Doppler waveforms. So what makes blood ow? In the simplest model of steady ow in a rigid tube, ow is related to a dierence

Fig. 1 Parabolic laminar ow. A narrow Doppler gate includes a narrow range of velocities, whereas a wide Doppler gate includes the full range of velocities within the vessel

Fig. 3 Pressure vs. ow. When laminar ow is present, increased pressure produces a linear increase in ow. However, when conditions produce turbulence, increases in pressure will produce diminishing increases in ow. Doppler waveforms will show spectral broadening (adapted from [1])

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between upstream pressure and downstream pressure by Poiseuilles law: DP = Q (8ln/pr4), where DP = the pressure drop along the vessel, Q = volume of ow, l = vessel length, n = uid viscosity, and r = vessel radius. The resistance to ow is expressed by (8ln/pr4). Thus, the most important factor in the resistance to ow is the radius of the vessel: for every 50% reduction in vessel radius, resistance to ow increases 16-fold. In physiologic situations, the small sub-millimeter arterioles contribute most of the resistance in in vivo vascular beds. In reality, blood ows because of dierences in uid energy between two points. Total uid energy is a summation of several components: pressure energy, kinetic energy, gravitational or potential energy, inertial energy (in pulsatile systems), and viscous energy (usually a form of energy loss). As with other forms of energy, Newtons laws of conservation apply. This becomes important when evaluating ow through a stenosis. The volume of ow (Q) through a vessel is the product of the mean velocity and cross-sectional area (Q = vA). When a narrowing is encountered, volume ow remains the same, which means that ow velocity must increase to account for the decreased cross-sectional area. In the idealized setting, uid owing through a stenosis loses no energy. Simplifying uid energy to be the sum of pressure and kinetic energy, means that the accompanying increased velocity through a stenosis is accompanied by a decrease in pressure such that: DP = p/2 (v22 ) v12), where DP = the pressure dierence, p = uid density, and v = velocity (Fig. 4). In vivo, how-

ever, there is often energy loss across a stenosis from inertial and viscosity losses (dissipated as heat). Losses will occur most markedly in tight stenoses where velocities are greatly accelerated, elevating the Reynolds number and producing increased energy losses due to inecient turbulent ow (Fig. 5). These energy losses across stenoses translate into decreased ow distal to the stenosis. At some point, energy loss becomes sucient to compromise ow to the end organ, and the stenosis becomes signicant or critical. By measuring velocities across a stenosis, we can estimate the pressure drop and thus infer compromise of downstream perfusion, which is the real clinical question. As mentioned, pulsatile ow in elastic vessels is a much more complicated phenomenon than steady ow in rigid pipes. However, for practical purposes and clinical application, the models work reasonably well. Some eects of the in vivo state are worth appreciating, however. The output of the left ventricle is highly pulsatile with rapid accelerations and decelerations. The compliance of an elastic vessel serves to store some of this energy during systole and release it more slowly during diastole [6], serving to decrease the pulsatility of the ow prole. This Windkessel phenomenon is well demonstrated in the aorta, with highly pulsatile ow in the ascending aorta giving way to less pulsatile more steady ow in the proximal abdominal aorta. Flow

Fig. 4 Theoretical ow through a stenosis, assuming no energy loss. The total energy of ow remains constant, but pressure energy decreases and kinetic energy (velocity) increases through the stenosis (adapted from [1])

Fig. 5 Flow through a critical stenosis. In vivo, ow through a stenosis results in inertial and viscous energy losses and, if severe enough, turbulent energy loss. This produces diminished total ow energy downstream of the stenosis, resulting in compromised perfusion (adapted from [1])

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pulsatility is also dependent upon the downstream impedance to ow. In the steady-state model, resistance to ow is proportional to 1/r4, but with pulsatile ow, the total impedance to ow increases, taking into account not only vessel diameter but also inertial forces and the reection of pressure waves from bifurcations. Again, the sub-millimeter arterioles are the most significant contributors to wave reections, and thus are the major determinant of downstream impedance [1]. Higher impedance gives rise to greater waveform pulsatility, whereas lower impedance gives lower pulsatility waveforms. In clinical practice, this pulsatility is characterized by a number of measures, including the resistive index [RI = (systolic v ) diastolic v)/systolic v], the pulsatility index [(systolic v ) diastolic v)/mean v], and the S/D ratio (systolic v/diastolic v). While the above discussion applies to arterial ow, venous ow is dierent. Since venous ow is less dependent upon arterial pulsatility (being isolated by the intervening capillary bed), venous ow depends more upon downstream pressure changes. Flow velocities are lower and more continuous, with laminar ow the norm and turbulent ow uncommon. Venous waveforms reect local eects of tissue pressure and changes in abdominal and thoracic pressure during respiration. The exception to this is the superior inferior vena cava (IVC) and the hepatic veins, whose waveforms are greatly inuenced by cardiac activity.

Arterial waveform analysis

The arterial waveform obtained at any given location reects upstream, local, and downstream factors. The waveform itself can be broken down into discrete characteristics: peak systolic velocity (PSV), end diastolic velocity (EDV), and pulsatility (Fig. 6). The systolic acceleration time (AT) or acceleration index (AI) measures how rapidly the PSV is reached from end diastole. How these components are altered can prove useful in interpreting Doppler waveforms, and depending upon

the clinical scenario they can either be normal, increased, or decreased. Proper measurement of PSV requires appropriate angle correction of the insonating beam. Insonating angles less than 60 degrees are generally regarded as adequate to obtain accurate measurements. The importance of a low angle of insonation lies not only in the production of a higher Doppler frequency shift, but the eect of angle measurement error on the measured frequency shift is lessened [7]. While the details are beyond the scope of this paper, the maximal detectable Doppler shift is equal to one-half of the pulse repetition or sampling frequency. If ow velocities exceed this rate, then aliasing will occur, where velocity signals will be displayed as lower values than they actually are. While this can create confusion during color Doppler interrogation, it can also be useful when searching for stenoses and areas of increased PSV. Peak systolic velocity is increased with increased volume ow, when there is ow through a stenosis, and for some distance just downstream of a stenosis. PSV increases will be less for long stenoses, and Bude and Rubin [8] have shown that the actual post-stenotic increase in PSV is also inversely related to downstream impedance. Decreases in PSV tend to occur downstream of a ow-limiting stenosis, but can also be seen with poor cardiac output. AT and AI are normally quite rapid; decreases can be seen in aortic stenosis, downstream of signicant stenoses, and in highly compliant vascular beds. Decreased early systolic acceleration (increased AT, decreased AI) also occurs as a normal function of increasing downstream cross-sectional area in an in vitro model [9] and probably occurs in vivo as well. EDV decreases as a result of downstream increased impedance to ow (vasoconstriction) and is reected in an increase in the RI. EDV increases in response to downstream decreased impedance to ow (vasodilatation). Additionally, EDV increases downstream of arterial stenoses of greater than 50% as diastolic pressure gradients develop. Increases in EDV are reected in decreased RI values.

Clinical applications
Liver Normal vasculature The portal vein is normally responsible for 7075% of blood ow to the liver, and is formed by the conuence of the splenic and superior mesenteric veins, dividing into right and left branches within the porta hepatis. Variants of intrahepatic portal venous branching occur in up to 20% of people [10, 11]. The portal vein diameter increases in size with age and weight [12] with newborn

Fig. 6 Waveform measures. PSV peak systolic velocity, EDV end diastolic velocity, AT acceleration time, the time from EDV to the early systolic peak

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diameters of 35 mm growing to 713 mm by age 20 [12, 13]. Portal vein ow is typically minimally phasic with constant ow toward the liver (hepatopetal) [11]; there are minor variations with cardiac pulsations and with respiration [1416]. Portal vein blood ow volume and ow velocity normally increases after meals [17], a reection of increased superior mesenteric arterial ow [18]. During fetal development, the ductus venosus forms a communication from the umbilical recess of the left portal vein to the inferior cava. While functional closure of the ductus venosus occurs shortly after birth in term infants, Doppler interrogation may show anatomic patency for as long as 3 weeks in term infants and over 1 month in preterm infants [1922]. Recognition of this normal structure is important to avoid confusion with intrahepatic shunts or varices [23]. The valveless hepatic veins drain into the IVC just below the right atrium (RA). Most people have a right, middle, and left hepatic vein, with one-third to one-half of people having at least one accessory vein [11]. The hepatic venous waveform is classically triphasic, with a characteristic retrograde A wave due to right atrial contraction. After atrial contraction, blood ows rapidly into the RA during diastole. At the start of ventricular systole, the tricuspid valve closes and even bulges into the RA, slowing the antegrade ow of blood (C wave, often not seen). During ventricular systole, blood rapidly ows toward the RA (S wave), slowing as the atrium lls. As ventricular diastole begins, the tricuspid valve opens (V wave) and ow towards the heart increases (D wave), slowing during the later part of diastole as the RA and right ventricle ll. At this point, atrial systole occurs, producing the retrograde A wave once again (Fig. 7) [16, 24, 25]. This pattern assumes normal thoracic pressures, cardiac function, and hepatic parenchymal compliance. However, this classic pattern occurs

in only 42% of healthy children, with the rest showing monophasic ow in at least one hepatic vein [26, 27]. Neonates often have monophasic ow, and food intake has no signicant eect on hepatic venous waveforms [26]. The middle hepatic vein is most commonly triphasic, and the right hepatic vein the least commonly triphasic, which may relate to eects of the angle of insonation as much as physiologic dierences [26, 27]. The hepatic artery provides 2530% of hepatic blood ow. The common hepatic artery arises from the celiac axis and becomes the proper hepatic artery after giving rise to the gastroduodenal artery. Running anteromedial to the common bile duct within the porta hepatis, the proper hepatic artery divides into right and left intrahepatic branches. Anatomic variants occur in almost half of the population [11], with the most common variant being a right hepatic artery arising from the superior mesenteric artery (SMA). Doppler interrogation demonstrates a typical visceral velocity prole with continuous forward diastolic ow and an RI of 0.60.7. Increases in hepatic arterial RI suggest increased intrahepatic impedance and hepatic disease. However, hepatic artery resistance also increases in response to food ingestion [11] and in the presence of vasoconstrictors. Portal hypertension The pressure gradient from the portal vein to the IVC is typically less than 5 mm Hg; when the pressure gradient exceeds this, portal hypertension is present [28]. Portal hypertension is generally divided into three types: presinusoidal or pre-hepatic (problems with portal vein inow), sinusoidal or intra-hepatic (hepatic parenchymal disorders), and post-sinusoidal or post-hepatic (problems with hepatic venous drainage) [11, 15, 28]. Pre-sinusoidal portal hypertension occurs when there is extrahepatic portal vein stenosis or occlusion, and accounts for at least 50% of pediatric portal hypertension [29]. Sinusoidal portal hypertension is caused by a wide array of disorders in children. Inltration due to metabolic diseases, congenital hepatic brosis, cystic brosis, and other diseases may all lead to cirrhosis and portal hypertension [11, 28, 30]. Post-sinusoidal portal hypertension results from obstruction to venous outow due to occlusion of the IVC and/or large hepatic veins (Budd-Chiari syndrome), or from obstruction of small intrahepatic venules and sinusoids (veno-occlusive disease). Children with portal hypertension may present with ascites, splenomegaly (with or without hypersplenism), hematemesis from variceal hemorrhage, distended collateral abdominal veins, and encephalopathy [11, 15, 28]. All forms of portal hypertension may demonstrate portosystemic collaterals, alterations of ow within the hepatic vasculature, as well as alterations in the appearance of the liver and spleen.

Fig. 7 Hepatic venous waveform and relationship to cardiac activity (adapted from [23])

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Abnormalities of portal vein ow occur because of increased vascular impedance due to abnormal vasculature or hepatic parenchyma. The portal vein often increases in size as portal pressure rises. However, the actual size of the portal vein is variable depending on the degree of collateral shunt ow and impedance to ow within the portal vein [15]. Portal hypertension is readily diagnosed when there is actual reversal of ow within the portal vein directed away from the liver (hepatofugal) (Fig. 8), although this is a very late and severe nding and can be caused by other hepatic vascular abnormalities [31]. Hepatofugal ow may be present in only certain intrahepatic portal venous branches either from variations in severity of parenchymal disease or from hepatic arteriovenous shunting known to occur in cirrhosis [31]. More typically, portal vein velocities (and by inference volume ow) decrease in the setting of portal hypertension, and the portal venous waveform becomes more pulsatile (Fig. 9) [3235]. Portal ow may actually cease or reverse with Valsalvas maneuver or breath-holding [36], and normal post-prandial ow increases are dampened [37]. Portal vein pulsatility is reported to be 94% sensitive for portal hypertension and a portal vein velocity of less than 20 cm/s is 6783% sensitive for cirrhosis [32, 34, 35]. Unfortunately, these ndings are less reliable with early or mild disease.

Fig. 9 Portal hypertension in a teenager with cystic brosis. Pulsatile portal venous waveforms with cessation of hepatopetal ow with inspiration

Fig. 8 Portal hypertension. An 8-year-old patient with end-stage liver disease and hepatofugal portal vein ow. Hepatopetal hepatic arterial ow is seen above the baseline

With decreased portal venous ow, there is a relative increase in hepatic arterial ow. The ratio of hepatic arterial to portal venous ow has been touted to be a good indicator of portal hypertension, with a ratio of more than 3 having a sensitivity between 75 and 78% [34, 35]. While hepatic arterial ow may be increased, continued hepatic parenchymal disease may lead to increased vascular impedance and thus decreased diastolic blood ow with increased waveform pulsatility. Hepatic venous waveforms are also aected by portal hypertension and intrinsic liver disease. Both reduced hepatopetal blood ow and decreased parenchymal compliance serve to dampen hepatic venous waveforms [34]. With increasing portal pressure, splanchnic blood must nd other avenues for return to the central circulation. The formation and identication of portosystemic collaterals (either tributary or developed [38]) is a very specic sign of portal hypertension [39]. Tributary collaterals normally drain into the portal venous system, but become enlarged and have retrograde ow with portal hypertension. These vessels include the mesenteric veins, short gastric, and left gastric (coronary) veins, which give rise to gastroesophageal varices [28]. Esophageal varices lie within and cause abnormal thickening of the lesser omentum, visible sonographically between the aorta and the left lobe of the liver. In the absence of other causes (obesity, adenopathy), a lesser omental thickness at the level of the celiac axis greater than 1.7 times the diameter of the aorta is associated with portal hypertension [40]. Doppler interrogation can sometimes show these tortuous channels and demonstrate their venous waveforms (Fig. 10). Developed collaterals are recanalized vessels that do not normally communicate with the portal venous system, and include paraumbilical, splenorenal, and splenoretroperitoneal pathways. Doppler can readily demonstrate paraumbilical collaterals arising from the left portal vein and demonstrate their hepatofugal ow. In this situation, proximal left portal venous ow is often hepatopetal, but is diverted away from the liver parenchyma through these collateral pathways. The presence of paraumbilical collaterals does not occur with pre-sinusoidal portal hypertension from portal vein occlusion, as this collateral route de-

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Fig. 11 Splenorenal shunt. Transverse color Doppler image show a prominent splenic vein draining into the left renal vein due to portal hypertension

Fig. 10 Esophageal varices in a child with presinusoidal portal hypertension. Longitudinal gray-scale (a) and color Doppler (b) images through the gastroesophageal junction show tortuous venous channels (arrows) in the lesser omentum between the aorta (A) and liver (L)

pends on ample left portal venous ow [28]. Splenic varices and splenorenal shunts are identied in the left upper quadrant, often accompanied by a dilated left renal vein with elevated ow velocities compared to the right renal vein (Fig. 11). In some cases, splenic vein ow is completely reversed, with blood shunted transsplenically to surface collaterals [41]. Gallbladder wall thickening can occur in the setting of portal hypertension from the eects of liver disease as well as pericholecystic varices [41, 42]. Doppler can demonstrate these vascular channels (Fig. 12), which occur more commonly with extrahepatic portal vein obstruction [43] (up to one-third of cases [41]) and represent portoportal collaterals that help to supply intrahepatic portal vessels [44].

Fig. 12 Gallbladder varices in a child with cavernous transformation of the portal vein. Transverse gray-scale (a) and power Doppler (b) images of the gallbladder (GB) show wall thickening with anechoic channels (arrows) shown to be vessels with power Doppler

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Portal vein thrombosis Portal vein thrombosis results from dehydration, sepsis, hypercoagulability, and omphalitis [45]. In neonates, left portal vein thrombosis may be seen either with [45] or without [29] umbilical vein catheterization, and may be asymptomatic. Neoplastic causes include hepatoblastoma and hepatocellular carcinoma. Patients may present with abdominal pain and splenomegaly, although the acute event is often unrecognized. Like thromboses elsewhere, acute clot appears hypoechoic and expands the vein, becoming smaller and more echogenic with time. Doppler imaging of the portal vein is generally reliable for the assessment of thrombosis [29], but may give false-positive results with very slow portal ow [11, 15] or partial thrombosis [46]. Echogenic thrombus within the main portal vein or its branches, with complete or partial occlusion at Doppler imaging, is readily seen in children, with a sensitivity over 95% [35, 39] (Fig. 13). The Doppler nding of arterial waveforms within portal vein clot indicates tumor thrombus. Additionally, hepatic arterial resistance may be reduced in patients with portal vein thrombosis [47]. In response to portal vein occlusion, recanalization and collateral channels develop within the porta hepatis (cavernous transformation of the portal vein) to reconstitute ow to the intrahepatic portal circulation within 620 days from the time of occlusion [44]. Sonography shows these small tortuous channels within the porta hepatis without a denable normal extrahepatic portal vein, with a sensitivity of nearly 100% [11, 48]. Doppler shows antegrade or bidirectional venous ow [11, 44, 48] (Fig. 14). In spite of these portoportal collateral anastomoses, reconstituted blood ow is usually insucient to support splenomesenteric ow, leading to portal hypertension and portosystemic collaterals [10, 44]. Venous obstruction Obstruction to hepatic venous outow may occur at the level of the IVC or major hepatic veins (Budd-Chiari syndrome) or at the level of small hepatic venules and sinusoids (veno-occlusive disease). Budd-Chiari syndrome is uncommon in children, manifesting acutely with abdominal pain, ascites, congestive hepatomegaly, and jaundice [15, 24, 49]. Predisposing factors include tumors that may invade the hepatic veins, hypercoagulability, cirrhosis, and congenital anomalies of the hepatic venous ostia or IVC webs [11, 15, 24, 50, 51]. US demonstration of thrombus within the involved vessels is the most direct method of diagnosis, although failure to visualize hepatic veins may occur in patients with cirrhosis or hepatomegaly [11]. Doppler evaluation may show absence of ow and evidence of venous shunting toward subcapsular collaterals or to a non-obstructed hepatic vein [24]. The caudate lobe often has a separate
Fig. 13 Portal vein thrombosis in a 13-year-old patient with Crohns disease. Longitudinal gray-scale (a) image through the portal vein (PV) shows low-level echoes with the right portal vein, dicult to identify as thrombus. Color Doppler image (b) clearly shows the thrombosed vessel

venous drainage, and is thus spared in Budd-Chiari syndrome. Enlargement of the caudate vein to over 3 mm may indicate venovenous shunting and infer the presence of Budd-Chiari syndrome, at least in adults [52]. Findings of portal hypertension due to acute hepatic congestion may also be observed. Hepatic veno-occlusive disease presents with similar clinical ndings as Budd-Chiari syndrome, but is diagnostically more challenging by US. Originally described as resulting from the ingestion of herbal tea or food containing pyrrolizidine alkaloids [24, 50], in developed countries it is usually the result of marrow-ablative

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Fig. 15 Hepatic veno-occlusive disease after bone marrow transplantation. Angle-corrected waveform of the middle hepatic vein early after bone marrow transplantation (a) shows preserved triphasic ow. After the onset of hepatic dysfunction (b), there is a dampened monophasic pattern with reduced ow velocity

Fig. 14 Cavernous transformation of the portal vein in a child with hypersplenism. Longitudinal gray-scale image (a) through the porta hepatis shows multiple hypoechoic channels (arrows) instead of a main portal vein. Duplex Doppler image (b) shows multiple vascular channels within the porta hepatis representing portal vein cavernous transformation. To-and-fro ow within these vessels indicates prehepatic portal hypertension

chemotherapy and/or radiation used to prepare for bone marrow transplantation [24, 53]. The injury occurs in the centrilobular zone of the liver, producing necrosis of hepatocytes and sinusoidal brosis with resultant narrowing and brosis of central veins [49]. Because the larger hepatic veins are not directly involved, some have advocated renaming this condition sinusoidal obstruction syndrome [24, 49]. Reports on the utility of grayscale and Doppler US in diagnosing veno-occlusive disease are conicting, and imaging may be no more diagnostically sensitive than clinical parameters [53].

Since the involved structures are too small to be directly visualized, one must look for secondary eects and infer the presence of veno-occlusive disease in the appropriate clinical setting. Hepatofugal ow within the main portal vein after bone marrow transplantation indicates venoocclusive disease with a specicity of 93% [54]. Unfortunately, this nding is only about 50% sensitive [54], and tends to be present in only the most severe cases [53]. Monophasic hepatic venous ow can be seen in a variety of hepatic diseases [24, 55] and can suggest venoocclusive disease [54], although given the frequency that monophasic ow can be seen in normal subjects [26, 27], a change from previously documented triphasic ow to monophasic ow in the same vessel is probably a better indicator (Fig. 15). Eects upon the hepatic artery are more variable. Hepatic arterial resistance is generally reported to increase [11, 54] as it does in many causes of diuse liver disease. However, there is at least one report of decreased resistance in children with hepatic dysfunction after bone marrow transplantation [56], and another reporting no dierence in transplant patients with or without veno-occlusive disease [53]. In spite of the diculties with the sonographic diagnosis of venoocclusive disease, it has been suggested that a normal examination has a negative predictive value of 8596% [54], and can be useful to exclude other problems such as biliary obstruction or inltrative hepatic lesions. Liver transplantation US is a valuable tool in the evaluation of the liver transplant patient, both before and after transplantation [57]. It is important to be aware of the anatomy and nature of the surgical procedures performed for both whole-liver and segmental grafts, as the complications

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and imaging appearances may dier. This has recently been well reviewed by other authors [5860]. While US is generally sucient for these evaluations, CT or MRI may be useful in problematic cases [61, 62]. Doppler US is used in the pre-transplant evaluation to document portal vein and IVC size and patency, to look for vascular or other visceral abnormalities [28], and to identify portosystemic shunts that may lead to impaired portal venous blood ow after transplantation [58]. Unlike the native liver, the newly transplanted liver is highly reliant upon the hepatic artery for perfusion and graft survival [11]. Thrombosis or stenosis of the hepatic artery is the most common vascular complication, occurring in 1040% of patients [11, 63, 64]. In the immediate post-transplant setting, this can lead to graft loss and retransplantation in up to 90% of patients [63, 65], with concomitant increases in morbidity and mortality [66]. Early detection of hepatic arterial complications allows elective surgical or interventional radiological hepatic arterial revision, improving graft function and survival [63, 64, 66], and avoiding later complications such as biliary strictures. The diagnosis of hepatic arterial thrombosis based on Doppler imaging is generally reliable, although false-negative results may occur if collateral vessels are mistakenly interrogated [67] and false-positive results may occur in very low-ow conditions [68]. The normal post-transplant hepatic artery should have a brisk systolic upstroke with a systolic AT of under 0.1 s [11, 57]. While the RI would be expected to be between 0.5 and 0.7 [57], in the immediate post-operative period it may be as high as 1.0 due to the eects of donor age, graft ischemia, or use of pressors [69], and does not necessarily indicate a hepatic arterial problem. Doppler imaging of hepatic arterial stenosis may reveal a low RI, and elevated hepatic arterial systolic ow velocity at the level of narrowing to more than 2 m/s [11, 70, 71]. The presence of a tardus parvus (delayed systolic AT and low PSV) waveform indicates impaired hepatic arterial perfusion with up to a 100% positive predictive value [64] (Fig. 16). If the main hepatic arterial trunk can be visualized, then this sign is specic for stenosis, but if the main hepatic artery cannot be seen, this waveform could be due to arterial thrombosis and collateral ow [64]. Portal venous complications are less common than hepatic arterial complications but include thrombosis, kinking, and development of stenosis. The challenge of tting a graft into the pediatric patient sometimes puts pressure on the highly collapsible portal vein causing narrowing, which may limit inow and lead to thrombosis. Portal vein stenosis occurs at anastomotic sites in about one-fth of patients, and appears to be more common with segmental transplants when vein interposition grafts are used [72]. US may disclose focal

Fig. 16 Hepatic artery stenosis 5 days after liver transplantation. Hepatic artery Doppler waveform (a) shows a tardus parvus pattern with delayed AT with a low PSV and abnormally elevated diastolic ow (low RI) indicating severe stenosis. Arteriogram (b) shows a tight long segment stenosis that required surgical revision

narrowing of the portal vein, and there may be poststenotic dilatation of the intrahepatic vessel. Doppler imaging will show turbulence and acceleration of ow through the stenotic segment (Fig. 17). Recognition of portal vein stenosis is important, as it can lead to portal hypertension and even portal vein thrombosis. Transhepatic portal venous angioplasty is a feasible procedure in children, improves portal inow, reduces portal pressure, and obviates surgery [58, 72]. Once portal vein thrombosis occurs, however, the likelihood of successful revascularization is much worse. The post-transplant hepatic vein waveforms should exhibit normal triphasic ow. As already noted, many factors aect this waveform, and monophasic ow can be seen in normal patients. However, the change of a previously triphasic hepatic vein pattern to a monophasic pattern has been associated with both hepatic vein stenosis [73] and acute graft rejection [74, 75]. Conversely, the presence of a triphasic hepatic venous waveform has a high negative predictive value in excluding stenosis or rejection [73, 74]. IVC narrowing and thrombosis can occur from compression by the transplant or at anastomoses. Direct visualization of thrombus or stenosis and Doppler ow turbulence and acceleration is possible with US [11].

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Fig. 18 Celiac axis in a patient with cutaneous hemangiomas and hepatic infantile hemangioma. Transverse color Doppler image of the aorta (A) shows an enlarged celiac axis (arrow) and common hepatic artery (arrowheads) due to shunting Fig. 17 Portal vein stenosis after liver transplantation. Color Doppler image of the portal vein (PV) after segmental liver transplantation shows a tight focal stenosis (arrow) producing acceleration of blood ow (2 m/s) with color Doppler aliasing (arrowheads) as well as post-stenotic intrahepatic portal venous dilatation

Liver tumors Although vascular invasion by a mass is strongly associated with malignancy, Doppler characteristics cannot be used to identify the type of tumor [76]. While malignant tumors tend to have high Doppler spectral shifts [77, 78], there is sucient overlap with benign infantile hemangioma (hemangioendothelioma) [79] to render it non-useful in an individual patient. Similarly, solitary infantile hemangiomas are often dicult to dierentiate from other masses in the absence of vessel enlargement [80] and from the rarer hepatic arteriovenous malformation [81]. The principal supply to both malignant tumors (such as hepatoblastoma and hepatocellular carcinoma) as well as benign vascular tumors (infantile hemangioma) is from the hepatic artery, although portal supply and portal shunting can also be found [79]. Arteriovenous shunting occurs in both benign and malignant lesions, which may produce enlargement of the celiac axis and hepatic arteries on gray-scale sonography with increased Doppler ow velocities [80] (Fig. 18). Patients with large shunts may present with hepatomegaly and high-output congestive failure. The abdominal aorta below the celiac artery may be reduced in size due to shunting. Doppler of the involved draining hepatic vein may show arterialized ow and higher ow velocity than hepatic veins uninvolved with the lesion [81] (Fig. 19). Doppler is 90% sensitive compared with arteriography in demonstrating direct vascular shunts, which has recently been reported to be predictive of the need for embolization therapy in symptomatic children [80]. Successful medical treatment

Fig. 19 Hepatic vein waveforms in infantile hemangioma. Anglecorrected middle hepatic vein waveform (a) shows a normal pattern. The hemangioma was drained via the left hepatic vein, whose waveform (b) shows increased pulsatility and ow velocity due to arterial shunting

or embolization of vascular liver masses can show reduction in lesional blood ow, and thus Doppler can be used to assess the ecacy of therapy [77, 79, 80]. Vascular malformations Nontumorous vascular malformations of the liver are rare. These malformations consist of abnormal communication between hepatic arterial, portal venous, and hepatic venous vessels as well as the IVC. Arterioportal shunts may be the result of trauma, interventional bili-

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ary procedures, tumors, cirrhosis, or may be congenital [10, 31, 82]. Doppler imaging can help demonstrate these direct arterioportal connections. The hepatic artery is typically enlarged, and there may be arterialization of the portal venous waveform. If the shunt is suciently large, there may be hepatofugal ow in that segment of portal vein and may even result in hepatofugal ow in the main portal vein [10, 31, 82]. While usually single, multiple arterioportal shunts have been described in association with hereditary hemorrhagic telangiectasia [83]. Portohepatic venous shunts may occur between the portal vein and hepatic vein or IVC. These shunts can be congenital [84, 85], perhaps due to a persistent vitelline vein [84]. Acquired shunts are usually due to liver disease and portal hypertension, and serve as collateral pathways for portal decompression [82]. Color Doppler can demonstrate the shunt, with large shunts showing a turbulent waveform whereas a smaller shunt may show elevated ow velocities through the narrow communication [82] (Fig. 20). Arteriohepatic venous shunts are

uncommon, but do occur with hereditary hemorrhagic telangiectasia [86]. Feeding hepatic arteries have elevated velocities and diastolic ow, and the draining hepatic veins are enlarged with pulsatile arterialized ow [82]. Portoportal shunts occur in the setting of extrahepatic portal vein occlusion and result in cavernous transformation of the portal vein, as described earlier. Similarly, hepatic venovenous shunts result from BuddChiari syndrome. Congenital extrahepatic portosystemic shunts are uncommon, and are often associated with cardiac, liver, biliary, renal, and skeletal abnormalities. These shunts are felt to arise due to aplasia or hypoplasia of the portal venous system during early development. Doppler US is useful in determining the presence or absence of the portal venous system, which has implications for therapy, although MRI may be necessary for a more global evaluation of shunt pathways [87]. Surgical shunts Surgical portosystemic shunts serve to decompress the portal venous system and treat complications from portal hypertension not controllable medically (variceal hemorrhage, ascites). Shunts may be created from the portal vein to IVC (portocaval), the splenic vein to left renal vein (splenorenal), or from a mesenteric vein to IVC (mesocaval). Non-surgical interventional radiology transjugular intrahepatic portosystemic shunts (TIPS) have also been successfully performed in children [88]. All shunts can be complicated by thrombosis or stenosis, and Doppler is the method of choice for evaluating patency [89]. Occasionally, mesocaval and splenorenal shunts may be dicult to evaluate due to intervening intestine [90]. Direct demonstration of ow across the shunt is the best indicator of patency. Indirect signs of shunt patency include hepatofugal portal vein ow, portosystemic collateral vessel decompression, and increased or turbulent ow in the recipient vessel [15]. TIPS shunts typically have high-velocity ow with spectral broadening. Velocity criteria for stenosis are variable [91], and comparison with immediate postprocedural baseline values may allow the best assessment of any signicant change [14].

Conclusion
The hemodynamics of owing blood are complex, but can be simplied by understanding a few main concepts such as conservation of ow, conservation of energy, laminar and turbulent ow, ow through a stenosis, and the contributions to impedance of vessel diameter and pulsatile ow. These principles govern the ow of blood, and thus the velocity vs. time tracing represented by the

Fig. 20 Congenital portohepatic shunt in an asymptomatic neonate. Color Doppler image (a) shows an abnormal communication with aliasing (arrow) between the portal vein (PV) and a hepatic vein (HV). Pulsed Doppler waveform (b) at the region of color aliasing shows abnormal velocity elevation to 1 m/s indicative of a stenotic venous communication

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Doppler US image. Knowing these principles allows understanding of their eects upon PSV, EDV, systolic AT, and pulsatility. Applying this knowledge to the clinical arena can greatly improve ones appreciation for the power of this technology, can improve ones understanding of patient physiology, and can hopefully

lead to better diagnostic capability. US is a powerful modality that avoids patient radiation exposure, does not require sedation, and can be performed portably in even the most critically ill patients. In an era of costconsciousness and radiation awareness, maximizing the use of US in pediatrics is especially desirable.

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