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Doppler Waveform of Hepatic Veins in Healthy Children

¹ Department of Pediatric Radiology, University Hospital of Geneva, Children's Hospital, 6 rue Willy Donzé, 1112 Geneva, Switzerland.
² Department of Pediatric Surgery, University Hospital of Geneva, 1112 Geneva, Switzerland.
³ Department of Pediatric Gastroenterology, University Hospital of Geneva, 1112 Geneva, Switzerland.

Received September 9, 1999; accepted after revision December 10, 1999.

 
Presented at the annual meeting of the Society for Pediatric Radiology, Vancouver, B. C., May 1999.

Address correspondence to S. Jequier.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. This study intends to document the presence or absence of triphasic waveforms in hepatic veins in healthy children. Does absence of triphasic hepatic vein flow indicate hepatic abnormality?

SUBJECTS AND METHODS. One hundred children without a known hepatic or intrathoracic abnormality underwent Doppler sonography of their hepatic veins. Fifty girls and 50 boys were divided into five age groups.

RESULTS. Forty-two children had triphasic flow in all three hepatic veins. Veins approaching an angle of 90° with the inferior vena cava could not be assessed or had the least flow modulations despite angle correction. Neonates had the highest percentage of monophasic flow (seven of 21) in all three hepatic veins and none had triphasic flow in all three veins.

CONCLUSION. Not all healthy children have a triphasic flow pattern in all hepatic veins. Before suspecting hepatic abnormality with abnormal parenchymal compliance (cirrhosis, graft rejection) by virtue of lack of triphasic hepatic vein flow, a normal variant of the flow should be considered. Only the change of a previously documented triphasic flow to monophasic flow in a given vein should be assessed as a sign of possible abnormality.

Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The hepatic veins drain blood from the low-pressure hepatic sinusoids toward the inferior vena cava. These veins are thin-walled anechoic vessels, have no valves, and are easily distinguished from the portal veins, which have echogenic walls. Flow in the hepatic veins is pulsatile, reflecting changes of blood flow through the right-sided heart chambers during the cardiac cycle. A normally occurring triphasic flow in the hepatic veins with reverse flow during atrial systole has been described [1]. This flow has been seen in healthy fetuses as early as in the second trimester [2]. For this venous backflow to occur, we assume that liver compliance must be normal. Liver parenchyma stiffening as seen in cirrhosis or in liver transplant rejection would lead to a loss of the triphasic venous flow. The ability to detect a hepatic parenchymal abnormality by hepatic venous Doppler studies is discussed by several authors. Their opinions vary considerably, some reporting these studies as valueless [3, 4], others documenting a high sensitivity and specificity in diagnosing cirrhosis [5] or liver transplant rejection [6]. Some of this confusion may be a result of the different methods used to assess venous hepatic flow. Some, mostly those claiming the flow analysis to be valueless, use the damp index (DI) measurement (DI = minimum velocity shift / maximum velocity shift) [3, 4], whereas others rely on the triphasic display of the flow as being normal and any change thereof as a sign of abnormality [5, 6].

To our knowledge, hepatic venous flow patterns have not been studied systematically in healthy children. We therefore undertook a prospective study of 100 children without known hepatic, cardiac, or pulmonary disease to document the frequency of triphasic, diphasic, or monophasic flow patterns in the three main hepatic veins, taking into account sex, age, activity, and the feeding state (fasting or postprandial) of each child.

Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
We prospectively examined the hepatic veins of 100 children without known hepatic disease or intrathoracic disease with Doppler sonography. This study was limited to the assessment of triphasic activity of hepatic vein flow in healthy children. No attempt was made to measure the velocity of the flow or to calculate hepatic vein flow volume in this population.

The children had been referred for abdominal sonographic examinations for the following reasons: urinary tract disease in 45 (pre- and postsurgery for obstructive lesions in 20; urinary tract infection in 11; follow-up of vesicoureteric reflux in five; microscopic hematuria in three; and renal dysplasia, oxaluria, varicocele, single umbilical artery, nephrocalcinosis, and screening for family cystic disease with negative result in one each); abdominal pain (without hepatic disease) in 17; remote oncologic disease in 10; search for pyloric stenosis in three; maternal oligamnios in four; maternal seroconversion for toxoplasmosis in four; annual (negative) checkup for HIV positivity or drepanocytosis in four; healthy children of colleagues (volunteers) in four; posttrauma in two; unconfirmed abdominal masses in two; and one each with a skin nodule, uncomplicated prematurity, postconvulsions, mild hydrocephalus, and cervical adenopathy. None of these children had known or subsequently established reasons for having any abnormal cardiovascular, pulmonary, or intraperitoneal process.

Fifty girls and 50 boys were divided into five age groups as illustrated in Table 1. They were examined in the supine position by an anterior approach or sometimes a lateral approach when no appropriate angle between the veins and the ultrasound beam could be obtained by an anterior approach. Scan heads (3.5-7 MHz) of a 128 XP (Acuson, Mountain View, CA) were chosen according to the patient's age and size. The factors age, sex, feeding status (fasting or postprandial), and activity (agitated, calm, or asleep) were recorded (Table 1). The variables were the Doppler flow pattern evaluation in the right, middle, and left hepatic vein in the liver venous drainage system. Accessory veins were ignored.

The sonographic flow pattern of the hepatic veins was graded as triphasic (Figs. 1A and 1B) when there was return of flow above the baseline of the spectral analysis curve, not considering whether ventricular systole was seen in addition to the atrial one. Flow was considered monophasic when there were no modulations seen other than respiration-related changes (Figs. 1C and 1D) and as diphasic when there were modulations that did not reach the baseline. Veins not found or flow pattern not interpretable were recorded as zero, equal to no signal.

View larger version (123K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —3-week-old male neonate with suspected but unconfirmed pyloric stenosis. Doppler sonograms of three hepatic veins reveal triphasic flow pattern in left hepatic vein by both anterior (A) and lateral (B) approaches and monophasic flow pattern in right (C) and middle (D) hepatic veins.

View larger version (109K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —3-week-old male neonate with suspected but unconfirmed pyloric stenosis. Doppler sonograms of three hepatic veins reveal triphasic flow pattern in left hepatic vein by both anterior (A) and lateral (B) approaches and monophasic flow pattern in right (C) and middle (D) hepatic veins.

View larger version (76K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —3-week-old male neonate with suspected but unconfirmed pyloric stenosis. Doppler sonograms of three hepatic veins reveal triphasic flow pattern in left hepatic vein by both anterior (A) and lateral (B) approaches and monophasic flow pattern in right (C) and middle (D) hepatic veins.

View larger version (82K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —3-week-old male neonate with suspected but unconfirmed pyloric stenosis. Doppler sonograms of three hepatic veins reveal triphasic flow pattern in left hepatic vein by both anterior (A) and lateral (B) approaches and monophasic flow pattern in right (C) and middle (D) hepatic veins.

The following events were evaluated because they were considered possible pitfalls affecting the sonographic measurements: Diaphragmatic excursions in rapidly breathing neonates and infants could be mistaken for reverse blood flow. Crying and sobbing might cause a Valsalva's maneuver and irregular diaphragmatic movements, which could change the spectral analysis curve. A patent sinus venosus (portocaval shunt) in neonates could simulate monophasic hepatic vein flow (Fig. 2A,2B,2C). Lastly, we avoided closeness of the ultrasound beam to cardiac muscles, which could cause transmission of movement of the cardiac wall to the hepatic veins and simulate triphasic flow. Doppler sonography was performed by two pediatric radiologists.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Patent ductus venosus in 3-day-old male neonate with mild hydrocephalus. Sagittal sonogram of liver shows patent ductus venosus (arrowheads) connecting left portal vein to inferior vena cava.

View larger version (88K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Patent ductus venosus in 3-day-old male neonate with mild hydrocephalus. Doppler sonogram of patent sinus venosus shows monophasic flow of higher velocity than that seen in C.

View larger version (133K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —Patent ductus venosus in 3-day-old male neonate with mild hydrocephalus. Doppler sonogram of middle hepatic vein reveals triphasic flow pattern.

For statistical analysis, variables and factors were evaluated one by one, two by two, and three by three for an analysis of variance for repeated measurements. The factors sex and age (between patients) and veins (within patients) and their interaction were tested a priori for significance. The factors movement and fasting and their interaction were tested a posteriori. The results are presented in the box plot (Fig. 3) and include the median (50th percentile), the box (25th and 75th percentiles), and the whiskers (10th and 90th percentiles). Outliers under the 10th and over the 90th percentile are included in the computations but are not reported. A cluster analysis in kappa-means clustering includes the factors sex and vein signal. The software Statistica (Statsoft, Tulsa, OK) for Windows (Microsoft, Redmond, WA) was used for analysis and graphs.

View larger version (23K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —Box plot of distribution of signal of flow in three hepatic veins revealed by Doppler sonography by percentile for age categories. () = right hepatic vein, () = middle hepatic vein, () = left hepatic vein. Distribution of flow patterns of each hepatic vein around median value is indicated by bars for children in 25th and 75th percentiles and by whiskers for children in 10th and 90th percentiles. Note that monophasic flow is much more common in neonates.

Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Analysis of the Flow Pattern
Forty-two percent of children had triphasic flow in all veins. The distribution of the flow pattern of each of the three main hepatic veins is summarized in Table 2.

There was a triphasic flow in two veins in 26%, triphasic flow in only one vein in 21%, and monophasic flow in all veins in 11% (mostly in neonates). Figure 1A,1B,1C,1D illustrates differences of flow amongst the three hepatic veins in a normal liver of a 3.5-week-old neonate. Only the left hepatic vein has a triphasic flow pattern. Unfavorable Doppler angle might account for poor Doppler tracing of the right, but not of the middle hepatic vein.

Of the three main hepatic veins, the middle vein revealed a triphasic flow pattern most consistently (Fig. 3). Dispersion was most marked in the right hepatic vein, which had the most variable flow pattern with 7% revealing no recordings, whereas the middle hepatic vein could be studied in almost all children (only 2% had no recording).

Statistical Analysis
Age proved to be highly significant. The large proportion of neonates in the group with only monophasic flow was the reason why they were separated as age group A from the other children less than 1 year old. Cluster analysis revealed an inhomogeneous pediatric population divided mainly by age, one having a triphasic vein flow pattern in at least one hepatic vein, the other (mostly neonates) having monophasic flow in all hepatic veins.

Compared with girls, boys had more triphasic flow in their right hepatic vein (p < 0.0005). This difference was greatest in the very young age group.

Fasting or recent ingestion of a meal as a single factor did not influence the hepatic vein flow pattern. A slight but statistically insignificant difference was seen in that children who were calm and fasting had more triphasic hepatic vein flow pattern (p < 0.0517).

Hepatic vein flow pattern as a single factor was not significantly different in children who were asleep, calm, awake, or agitated. A slight but statistically insignificant difference was seen in that children who were calm had a better triphasic flow pattern (p < 0.0505).

The only apparently significant interaction was between fasting and activity. Children who were both calm or asleep and fasting had more often a triphasic flow pattern than those who were calm or asleep but had just eaten (p < 0.0028).

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Hepatic vein flow patterns have been studied frequently in the adult population. A triphasic flow with backflow during right atrial and right ventricular contraction has been reported in healthy volunteers and proven by simultaneous registration of the Doppler waveform and its spectral analysis and by electrocardiography and phonocardiography [1]. Hepatic parenchymal disease such as cirrhosis or liver transplant rejection has been associated with loss of this triphasic hepatic venous flow [7, 8]. Influences of cardiac function, intraabdominal pressure, and intrathoracic pressure on hepatic vein flow pattern have also been reported. They affect not only the velocity of hepatic vein flow, but also the pulsatility. Pulmonary venous hypertension and increased pressure in the right heart chambers will increase hepatic vein pulsatility [9], whereas increased thoracic pressure (Valsalva's maneuver) will slow down the venous return to the right heart and diminish the pulsatility of the hepatic veins [10]. We therefore excluded all children with hepatic, pulmonary, or cardiac disease from the study.

Food intake is well-known to influence flow in the portal system of the liver. Flow increases in the portal vein and decreases in the hepatic artery after a meal. There was no significant difference of triphasic activity of hepatic vein flow pattern between children who were fasting and those who had just eaten. Again, the overall hepatic vein flow volume was not measured.

Activity will influence the entire circulation by accelerating cardiac output. In our population of healthy children, there was no significant difference of triphasicity of hepatic vein flow between children who were agitated, calm, or even asleep.

There was an apparent interaction between children who were fasting and calm compared with children who had just eaten and were calm, the latter having less triphasic flow than the former. This finding is probably a result of a bias in patient selection. Young children were mostly referred with urinary tract problems such as prenatally detected obstruction. Parents were routinely instructed to feed the babies before the sonographic examination to ensure good diuresis and good filling of the upper and lower urinary collecting systems. Older children were often referred for follow-up of remote hematooncologic disease. They would arrive fasting, because they usually also had a routine blood test just before or after the sonography. Crying and agitation are more frequent in young children. None of the adolescents was agitated, as illustrated in Table 1.

Besides the highly significant difference of triphasic activity between the three main hepatic veins, the second most significant difference found in the hepatic vein flow pattern was between the different age groups. A very large proportion of neonates had monophasic flow. This may explain the interaction with less triphasic flow pattern in patients who were fed and agitated because they were mostly neonates or infants, compared with those who were fasting and calm and were mostly adolescents.

We can only speculate as to a possible cause of monophasic hepatic vein flow pattern in neonates. The anatomy of the liver is different during young age [11], the liver being relatively large and horizontal in the abdomen and also hematopoietic, which may alter the liver compliance. The sinus venosus between the left portal vein and the vena cava closes later than the ductus arteriosus between the aorta and pulmonary artery [12], staying open for several days. The former represents a portocaval shunt that could theoretically influence the overall liver perfusion and liver compliance. In our study population, we had neonates with patent ductus venosus with a relatively high-velocity monophasic flow and triphasic hepatic vein flow pattern, which seems to contradict this hypothesis. It is not the purpose of this study to enter this debate, especially considering we did not check systematically for an open ductus venosus in all neonates.

The large variability of hepatic vein flow from one vein to another is surprising. Shapiro et al. [13] found flattened hepatic vein tracings in seven of 68 healthy patients, studying only the middle hepatic vein, confirming a certain variation within a healthy population.

Zero flow or uninterpretable flow was recorded 19 times: in seven right hepatic veins, two middle, and 10 left hepatic veins. This is similar to the results of Bombelli et al. [14], who studied flow velocities of all hepatic vessels, had difficulties with the hepatic veins only, and could not get hepatic vein flow measurements of all three veins in six of 22 healthy adult volunteers. These investigators did not specify which veins were difficult to examine.

In our patients, the middle hepatic vein had the most consistent triphasic flow, perhaps as a result of the most favorable Doppler angle.

Both the right and left hepatic veins can have an almost horizontal course with an unfavorable Doppler angle. Scanning by lateral approach sometimes helped to get a better spectral analysis curve of the Doppler study but did not change the flow pattern from monophasic to triphasic. As illustrated by Figure 1A,1B,1C,1D, the Doppler angle alone cannot account for all differences in flow between the three hepatic veins. More studies on the hepatic venous flow are needed for better comprehension of the different flow patterns in the same liver from one vein to another.

The slightly different hepatic vein flow pattern of each sex, affecting only the right hepatic vein, has no explanation. Statistically, the difference was minimal.

The present study in healthy children was performed to establish norms of flow pattern in the hepatic veins in children with no known disease process that might affect those flow patterns. The noted results can be used to assess the true value of certain questioned abnormal flow patterns in patients with suspected hepatic abnormality.

A logical consequence of our study would be the call for prudence in assuming that monophasic hepatic vein flow pattern is necessarily abnormal. In children, particularly in young ones, only the changes from documented triphasic flow to monophasic flow in a given vein should alert the sonographer to consider the possibility of active hepatic parenchymal disease such as liver graft rejection.

References

Top Abstract Introduction Subjects and Methods Results Discussion References

 

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