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Hepatic Arterial Diameter Measured with US: Adjunct for US Diagnosis of Biliary Atresia¹

¹ From the Departments of Radiology (W.S.K., J.E.C., B.J.Y., S.Y.Y., W.Y.K., I.O.K., K.M.Y.), Pediatrics (J.K.S.), and Surgery (K.W.P.), Institute of Radiation Medicine, Seoul National University College of Medicine, and Clinical Research Institute, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea. From the 2003 RSNA Annual Meeting. Received June 24, 2006; revision requested August 30; revision received December 14; accepted January 16, 2007; final version accepted March 20. Address correspondence to J.E.C. (e-mail: cheonje{at}snu.ac.kr).

	ABSTRACT

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Purpose: To prospectively evaluate the accuracy of hepatic artery diameter and hepatic artery diameter–to–portal vein diameter ratio for ultrasonographic (US) diagnosis of biliary atresia, with cholangiographic or clinical information as reference standard.

Materials and Methods: Institutional review board approval and informed consent were obtained. US was performed in 68 neonates and infants with cholestatic jaundice (mean age, 61 days; male-to-female ratio, 38:30). Biliary atresia (n = 38) was confirmed with cholangiography, and hepatitis (n = 30) was diagnosed with clinical (n = 24) or cholangiographic (n = 6) findings. Diameter of the right hepatic artery was measured with US. Right hepatic artery diameter–to–right portal vein diameter ratio was measured to determine relative enlargement of the hepatic artery. As a control group, 17 neonates and infants (mean age, 67 days; male-to-female ratio, 12:5) without jaundice underwent US of the porta hepatis. Statistical analysis was performed to compare US parameters among three groups with one-way analysis of variance. Optimal cutoff values of the hepatic artery diameter and hepatic artery diameter–to–portal vein diameter ratio for biliary atresia diagnosis were obtained with receiver operating characteristic analysis.

Results: The diameter of the right hepatic artery in biliary atresia group (1.9 mm ± 0.4 [standard deviation]) was significantly larger than that in the hepatitis (1.4 mm ± 0.3) and control (1.2 mm ± 0.2) groups (P < .001). Hepatic artery diameter–to–portal vein diameter ratio in the biliary atresia group (0.52 ± 0.12) was larger than that in hepatitis (0.40 ± 0.07) and in control (0.40 ± 0.10) groups (P < .001). Optimum cutoff values for diagnosis of biliary atresia were 1.5 mm (sensitivity, 92%; specificity, 87%; accuracy, 89%) for hepatic artery diameter and 0.45 for hepatic artery diameter–to–portal vein diameter ratio (sensitivity, 76%; specificity, 79%; accuracy, 78%).

Conclusion: Measurement of hepatic artery diameter can be helpful in the US diagnosis of biliary atresia.

© RSNA, 2007

	INTRODUCTION

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Biliary atresia and neonatal hepatitis are two important causes of hyperbilirubinemia in the neonatal period (1). The distinction between these two disorders is important because the prognosis and management of these clinical entities differ substantially. In patients with biliary atresia, early surgical intervention is essential. It is well known that the Kasai procedure (portoenterostomy) for biliary atresia can result in better clinical outcome when performed early in life (1–3). In patients with neonatal hepatitis, correct diagnosis may avoid unnecessary surgery. Therefore, it is important to determine accurately the cause of persistent neonatal jaundice as early as possible. However, making a presurgical diagnosis is sometimes difficult with the available diagnostic procedures, including hepatic scintigraphy with technetium 99m–diisopropyl iminodiacetic acid (4–7), ultrasonography (US) (8–15), and magnetic resonance cholangiography (16,17).

Among infants with cholestasis, US has been accepted as an initial imaging modality of choice to exclude visible obstructing lesions in the biliary trees and to differentiate biliary atresia from neonatal hepatitis (8–15). For the diagnosis of biliary atresia, US examination is used for determining the length, shape, and contractility of the gallbladder (8–10). Since the report by Choi et al (11) of "triangular cord" sign for the diagnosis of biliary atresia, US evaluation of the porta hepatis has become an important component of the US examination in these infants (11–15). Hypertrophy of the hepatic artery in biliary atresia has been noted at presurgical angiography for liver transplantation (18) or at histopathologic study (19,20). During US of the porta hepatis in patients with neonatal cholestasis, we have observed a large hepatic artery in patients with biliary atresia. Thus, the purpose of our study was to prospectively evaluate the accuracy of hepatic artery diameter and ratio of the hepatic artery diameter to the portal vein diameter for the diagnosis of biliary atresia at US, with surgical cholangiography or clinical information used as the reference standard.

	MATERIALS AND METHODS

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Patients
Institutional review board approval was obtained for this study. Although the need for informed consent was waived because of minimal risk, we did obtain it by informing the parents of our research study before they consented to our proceeding with US. From July 1999 to December 2005, 119 consecutive neonates and young infants who were clinically suspected of having biliary atresia or neonatal hepatitis because of persistent jaundice underwent hepatobiliary US. Of these, 25 patients with unconjugated hyperbilirubinemia related to breast feeding or prematurity with or without parenteral nutrition were excluded. We also excluded two infants with choledochal cyst, six patients with histologically confirmed Alagille syndrome, and 18 infants who were lost to follow-up. As a result, 68 infants with neonatal jaundice were included in our study (mean age, 61 days; male-to-female ratio, 38:30).

Biliary atresia was confirmed with surgical cholangiography in 38 patients (mean age, 64 days; male-to-female ratio, 16:22). Neonatal hepatitis was diagnosed according to clinical improvement during the follow-up period (evidenced by the patient's recovery from jaundice and normalization of laboratory values) in 24 patients or according to surgical cholangiography in six patients (mean age of these 30 patients, 57 days; male-to-female ratio, 22:8) (Fig 1). Although there was no significant difference in age (t test, P = .484) or body mass index [weight in kilograms/height in meters squared] (t test, P = .312) between patients with biliary atresia and those with neonatal hepatitis, the two groups differed by sex distribution (Fisher exact test, P = .017). In addition, although total serum bilirubin (t test, P < .001), direct bilirubin (t test, P < .001), and -glutamyl transferase (t test, P < .001) levels differed significantly between the patients with biliary atresia and those with neonatal hepatitis, there was no significant difference in serum alkaline phosphatase, alanine aminotransferase, or aspartate aminotransferase levels (Table 1).

View larger version (19K): [in this window] [in a new window] [Download PPT slide]   Figure 1: Flow diagram of inclusion criteria of patients.

US Techniques
After a minimum 4-hour fast, all patients underwent US with the use of 5–10-MHz transducers (HDI 3000 and HDI 5000, Advanced Technology Laboratories, Bothell, Wash; LOGIQ 9, GE Medical Systems, Milwaukee, Wis). US was performed independently by one of three pediatric radiologists (who had 10 [W.S.K.]), 5 [J.E.C.], and 3 [S.Y.Y.] years of experience with pediatric US at the time each first evaluated the study subjects). Diameter of the hepatic artery was measured at the level of right proximal hepatic artery running parallel to the right portal vein (Fig 2). For consistency, measurement was obtained at the level of the proximal portion of the right portal vein just proximal to the division of the anterior and posterior branches; this area was chosen because the anatomic locations of the hepatic artery and portal vein are more constant in the right lobe of the liver (21). Measurement was made by using an electronic caliper from the midportion of the anterior wall of the hepatic artery to the midportion of the posterior wall of the hepatic artery. We obtained the ratio of the diameter of the right hepatic artery to the diameter of the right portal vein to determine the relative enlargement of the hepatic artery.

View larger version (127K): [in this window] [in a new window] [Download PPT slide]   Figure 2a: US images of measurement of hepatic artery diameter at proximal right hepatic artery. Diameter of hepatic artery is measured at level of proximal right hepatic artery running parallel to right portal vein. (a) Oblique scan obtained along the course of portal vein shows enlarged hepatic artery (arrowheads) in biliary atresia compared with (b) artery (arrows) seen on scan obtained in control subject.

View larger version (116K): [in this window] [in a new window] [Download PPT slide]   Figure 2b: US images of measurement of hepatic artery diameter at proximal right hepatic artery. Diameter of hepatic artery is measured at level of proximal right hepatic artery running parallel to right portal vein. (a) Oblique scan obtained along the course of portal vein shows enlarged hepatic artery (arrowheads) in biliary atresia compared with (b) artery (arrows) seen on scan obtained in control subject.

Statistical Analysis
Normal distribution of the data for the US parameters was assessed with the Kolmogorov-Smirnov test. Between groups, statistical differences were compared by using one-way analysis of variance with a Scheffe post hoc test. The ² test was used to assess categoric data (presence or absence of triangular cord sign, common bile duct, biliary cyst, and hepatic artery enlargement).

To determine the diagnostic performance of the hepatic artery diameter and the ratio of the hepatic artery diameter to the portal vein diameter in the diagnosis of biliary atresia, receiver operating characteristic (ROC) analysis was performed. Thirty-eight patients with biliary atresia and 47 patients without biliary atresia (30 patients with neonatal hepatitis and 17 control subjects) were included in the ROC analysis. Areas under the ROC curves with 95% confidence intervals were calculated for the hepatic artery diameter and the ratio of the hepatic artery diameter to the portal vein diameter. Cutoff values (values higher than the cutoff values indicate positivity for biliary atresia) for each US parameter, which were balanced between sensitivity and specificity (ie, minimal false-negative and false-positive results), were determined by selecting the nearest coordinate on each ROC curve to the left upper corner (ie, 0, 1) of the ROC graph. The sensitivities and specificities of each cutoff value were calculated for each criterion for size of the hepatic artery.

We evaluated the sensitivity and specificity of other US findings of biliary atresia in the porta hepatis (triangular cord sign and nonvisualization of the common bile duct, respectively), both singly and as a combination with the preceding criteria for hepatic artery size, to assess the diagnostic accuracy added with measurement of the absolute and the relative size of the hepatic artery.

Statistical analysis was performed with software (SPSS for Windows, version 11.5; SPSS, Chicago, Ill). A two-tailed P value less than .05 was considered to indicate a statistically significant difference.

	RESULTS

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Hepatic Artery
The diameter of the right hepatic artery in patients with biliary atresia (1.9 mm ± 0.4 [standard deviation]) was significantly larger than that in patients with neonatal hepatitis (1.4 mm ± 0.3) (P < .001) and that in control subjects (1.2 mm ± 0.2) (P < .001) (Table 2, Fig 3a). The ratio of the hepatic artery diameter to the portal vein diameter in patients with biliary atresia (0.52 ± 0.12) was significantly larger than that in patients with neonatal hepatitis (0.40 ± 0.07) (P < .001) and control subjects (0.40 ± 0.10) (P < .001) (Fig 3b). The diameter of the portal vein did not significantly differ between the biliary atresia group (3.8 mm ± 0.7) and the neonatal hepatitis group (3.5 ± 0.6) (P = .488). There were no significant differences in the hepatic artery diameter (P = .067), the portal vein diameter (P = .309), or the ratio of the hepatic artery diameter to the portal vein diameter (P = .976) between the neonatal hepatitis group and the control group.

View larger version (12K): [in this window] [in a new window] [Download PPT slide]   Figure 3a: Scatterplots of (a) hepatic artery diameter and (b) ratio of hepatic artery diameter to portal vein diameter in biliary atresia, neonatal hepatitis, and control groups. Differences in hepatic artery diameter and ratio of hepatic artery diameter to portal vein diameter were significant. Dotted line indicates (a) 1.5-mm diameter criterion and (b) 0.45 ratio criterion.

View larger version (8K): [in this window] [in a new window] [Download PPT slide]   Figure 3b: Scatterplots of (a) hepatic artery diameter and (b) ratio of hepatic artery diameter to portal vein diameter in biliary atresia, neonatal hepatitis, and control groups. Differences in hepatic artery diameter and ratio of hepatic artery diameter to portal vein diameter were significant. Dotted line indicates (a) 1.5-mm diameter criterion and (b) 0.45 ratio criterion.

	DISCUSSION

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At US, the hepatic artery and portal vein are easily detectable structures in the porta hepatis, and their diameters can be measured with the electronic caliper of the US machine. Our study results showed that US depicted an enlarged hepatic artery in the biliary atresia group; it was significantly larger than that in the neonatal hepatitis and the control groups. The criterion of enlarged hepatic artery diameter (>1.5 mm) showed a sensitivity of 92%, a specificity of 87%, and an accuracy of 89% in the diagnosis of biliary atresia. The ratio of the hepatic artery diameter to the portal vein diameter (>0.45) provided a sensitivity of 76%, a specificity of 79%, and an accuracy of 78%. These results suggest that hepatic artery enlargement can be used as one of the US findings of biliary atresia. However, hepatic artery enlargement was seen in six patients (20%) with neonatal hepatitis. We assumed that this finding might be a secondary change of the hepatic artery due to prolonged hepatic inflammation.

In US diagnosis of the biliary atresia, an atretic gallbladder that appears small, has an irregular contour, and lacks echogenic mucosal lining has been accepted as a characteristic finding of biliary atresia (8–10). Several reports (11–15) have addressed the importance of US of the porta hepatis. In the evaluation of the porta hepatis in patients with neonatal jaundice, the triangular cord sign (originally defined as a triangle- or tube-shaped, highly reflective area just cranial to the portal vein bifurcation on transverse or longitudinal scans) has been claimed to be a sensitive and specific indicator of biliary atresia (11). In our experience, the brightness and thickness of the triangle-shaped reflective area at the portal vein bifurcation varied; therefore, it was sometimes difficult to define triangular cord sign without objective measurement. According to the article by Lee et al (12), objective criteria of the triangular cord thickness (thickness of anterior wall of the right portal vein >4 mm) may be useful in the evaluation of the triangular cord sign (sensitivity, 80%; specificity, 98%). However, use of the triangular cord sign has limitations. According to Tan Kendrick et al (9), the triangular cord can be masked in the presence of diffuse periportal echogenicity due to nonspecific inflammation or cirrhosis. In addition, thickened periportal echogenicity can be seen in patients with neonatal hepatitis and other liver parenchymal diseases (13). In our study, the triangular cord sign was very specific but less sensitive than other US findings of the porta hepatis (specificity of 93% and sensitivity of 58% for the diagnosis of biliary atresia). Sensitivity was lower than that reported elsewhere (range, 80%–95%) (11–13).

Regarding the US demonstration of the extrahepatic bile duct in the porta hepatis, Azuma et al (15) reported that absence of the common bile duct at US was considered a positive criterion for biliary atresia (sensitivity, 83%; specificity, 71%). However, evaluation of the common bile duct alone also has limitations. In assessing the common bile duct in neonates or young infants, the critical factor is the size of the common bile duct. The duct is a distensible or collapsible structure responsive to fluctuations in prandial bile flow, and the mean diameter of the common bile duct was reported to be 0.69 mm ± 0.48 in patients 3 months or younger (24). In our experience, it was frequently difficult to demonstrate a "normal" common bile duct with US in this age group. We think, therefore, that the evaluation of the common bile duct alone may induce false-positive results for US diagnosis of biliary atresia. However, false-negative cases can also occur because a patent or dilated extrahepatic bile duct can be seen in some patients with biliary atresia (14,25). In our study, the common bile duct criterion (nonvisualization of the common bile duct) resulted in six (20%) false-positive results (nonvisualization of the common bile duct in patients with neonatal hepatitis) and two (5%) false-negative results (visualization of the common bile duct in patients with biliary atresia).

Each US finding of the porta hepatis (the triangular cord sign, bile cysts, nonvisualization of common bile duct) can be useful in the US diagnosis of biliary atresia despite the limitations of this modality. We think that a finding of an enlarged hepatic artery may help enhance diagnostic accuracy of biliary atresia when combined with known US findings of the porta hepatis. In our study, the best combination of US findings was nonvisualization of the common bile duct and an enlarged hepatic artery, with a sensitivity of 89%, a specificity of 96%, and an accuracy of 93%.

Our study had several limitations. First, although recent advances in US equipment allow detection and measurement of submillimeter structures, US measurement error may result from the small size of the hepatic artery. Second, although the anatomy of the right hepatic lobe is more constant and we were consistent when selecting the site of measurement, anatomic variation of the hepatic artery may exist and implicate a limitation of measurement. Third, although the mean diameter of the hepatic artery in older children (mean age, 6.0 years) was reported to be 2.29 mm ± 0.91 (24), to our knowledge there are no accepted standards to define the normal size of the hepatic artery in neonates and young infants. Although we provided "normal" data of the hepatic artery diameter in this age group, the number of control subjects was not large. Further prospective study for the standard value of the hepatic artery diameter in this age group may provide useful information in the differential diagnosis of biliary atresia and neonatal hepatitis.

In conclusion, hepatic artery diameter can be helpful in the US diagnosis of biliary atresia—combined with other US findings, enlargement of the hepatic artery can be highly suggestive of biliary atresia. We believe that measurement of the hepatic artery diameter is an important component of the US diagnosis of biliary atresia.

	ADVANCE IN KNOWLEDGE

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• Enlargement of the hepatic artery diameter (>1.5 mm at the level of proximal right hepatic artery) can be helpful in the US diagnosis of biliary atresia.
  

	IMPLICATION FOR PATIENT CARE

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• Combined with other US findings, enlargement of the hepatic artery can be highly suggestive of biliary atresia.
  

	FOOTNOTES

 

Abbreviations: ROC = receiver operating characteristic

Author contributions: Guarantors of integrity of entire study, W.S.K., J.E.C.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, W.S.K., J.E.C., B.J.Y., K.M.Y.; clinical studies, W.S.K., J.E.C., B.J.Y., S.Y.Y., W.Y.K., I.O.K., J.K.S., K.W.P.; statistical analysis, J.E.C.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.

	References

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2452061093v1 245/2/549    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kim, W. S. Articles by Park, K.-W. Search for Related Content PubMed PubMed Citation Articles by Kim, W. S. Articles by Park, K.-W.