Pediatric Radiology

, Volume 33, Issue 9, pp 614–620

Congenital extrahepatic portosystemic shunts

Authors

  • Conor P. Murray
    • Department of Diagnostic ImagingHospital for Sick Children
    • Department of Diagnostic ImagingHospital for Sick Children
  • Paul S. Babyn
    • Department of Diagnostic ImagingHospital for Sick Children
Original Article

DOI: 10.1007/s00247-003-1002-x

Cite this article as:
Murray, C.P., Yoo, S. & Babyn, P.S. Pediatr Radiol (2003) 33: 614. doi:10.1007/s00247-003-1002-x

Abstract

Background

A congenital extrahepatic portosystemic shunt (CEPS) is uncommon. A type 1 CEPS exists where there is absence of intrahepatic portal venous supply and a type 2 CEPS where this supply is preserved. The diagnosis of congenital portosystemic shunt is important because it may cause hepatic encephalopathy.

Objective

To describe the clinical and imaging features of three children with CEPS and to review the cases in the published literature.

Materials and methods

The diagnostic imaging and medical records for three children with CEPS were retrieved and evaluated. An extensive literature search was performed.

Results

Including our cases, there are 61 reported cases of CEPS, 39 type 1 and 22 type 2. Type 1 occurs predominantly in females, while type 2 shows no significant sexual preponderance. The age at diagnosis ranges from 31 weeks of intrauterine life to 76 years. Both types of CEPS have a number of associations, the most common being nodular lesions of the liver (n=25), cardiac anomalies (n=19), portosystemic encephalopathy (n=10), polysplenia (n=9), biliary atresia (n=7), skeletal anomalies (n=5), and renal tract anomalies (n=4).

Conclusion

MRI is recommended as an important means of diagnosing and classifying cases of CEPS and examining the associated cardiovascular and hepatic abnormalities. Screening for CEPS in patients born with polysplenia is suggested.

Keywords

Congenital extrahepatic portosystemic shuntMagnetic resonance imagingHepatic nodular hyperplasiaPolyspleniaLeft isomerism

Introduction

The clinical importance of congenital extrahepatic portosystemic shunts (CEPSs) is in their associations, particularly liver and cardiac abnormalities, and because they may cause hepatic encephalopathy. Two types of congenital portosystemic shunt exist: intrahepatic and extrahepatic [1, 2]. This report is concerned with CEPS and excludes intrahepatic shunts such as congenital hepatic vascular lesions and persistent patency of the ductus venosus. CEPS has been classified into two main types depending on the presence or absence of intrahepatic portal venous supply (Table 1). We report three cases of CEPS, stressing the importance of magnetic resonance imaging, and summarize the available literature.
Table 1.

Classification of congenital extrahepatic portosystemic shunts (after [3])

Type 1. With absence of intrahepatic portal veins

  1a. Superior mesenteric and splenic veins do not join to form extrahepatic portal vein

  1b. Superior mesenteric and splenic veins join to form a short extrahepatic portal vein

Type 2. With patent intrahepatic portal veins

Materials and methods

Three patients with CEPS presented to our institution during a 5-year period. For each case the parameters evaluated were age and sex, clinical presentation, route and drainage of the shunts, thoracoabdominal visceral situs and splenic status, associated anomalies, presence of focal liver disease, liver function tests and serum ammonia, clinical management and outcome, and future treatment planned (see Table 2). All three patients were investigated with magnetic resonance imaging, transabdominal ultrasonography, and abdominal computed tomography. Patients 1 and 3 underwent X-ray angiography. Patients' clinical data were obtained from the medical charts. In addition, an extensive literature review of English language journals and textbooks published between 1793 and 2002 was made through the search capabilities of the National Library of Medicine Ovid online database using the keywords 'shunt', 'portosystemic shunt', 'splenorenal shunt', and 'portocaval shunt'. Further information was gathered from the relevant authors via mail where data were absent or ambiguous.
Table 2.

Summary of patient data

Parameter

Patient number

1

2

3

Age/sex

3 month old/female

18 month old/female

4 year old/male

Presentation

Acute respiratory distress requiring ICU admission

Rectal bleeding and peripheral edema

Follow up post biliary diversion in infancy

Type of shunt

Type 2

Type 1

Type 2

Route of shunt

Spleno-left renal

Spleno-left renal

Spleno-right renal

Visceral situs and splenic status

Heterotaxy with polysplenia and interruption of inferior vena cava

Solitus with normal spleen and normal inferior vena cava

Heterotaxy with polysplenia and interruption of inferior vena cava

Liver lesions

Three nodular lesions

A focal nodular lesion

Focal nodular hyperplasia, hepatoblastoma

Liver function tests

Hepatic function normal

Hypoalbuminemia normal

Hepatic function normal

Elevated transaminases

Elevated transaminase

Elevated transaminases

Serum ammonia normal

Serum ammonia normal

Serum ammonia elevated

Other associations

Pulmonary hypertension

Juvenile polyposis defect

Biliary atresia

Translocation 2,10

Ventricular septal defect

Atrial septal defect

Outcome

Right heart failure

Persistent rectal bleeding and anemia

Liver transplant performed

Developmental delay

Palliative management

Developmental delay

Results

Patient 1

A 3-month-old girl was admitted to the intensive care unit with respiratory distress and pulmonary hypertension unresponsive to medical therapy. Echocardiography demonstrated a dilated, poorly functioning right ventricle in association with polysplenia, interruption of the inferior vena cava with azygos continuation, and left atrial isomerism. No additional cardiac defect was found. Abdominal ultrasound demonstrated ill-defined echogenic lesions in the peripheral parts of the liver, and the portal vein could not be identified. Magnetic resonance imaging of the chest and abdomen with contrast-enhanced angiography demonstrated three nodular liver lesions (Fig. 1). There was no evidence of pulmonary venous obstruction. As an incidental finding, a large fistulous tract was identified between the splenic vein and left renal vein. The portal vein was very small. Subsequent celiac arteriography demonstrated a hypoplastic, 'corkscrew' portal vein in the venous phase. Serum biochemistry revealed a transient, marked elevation in liver transaminase levels with preservation of synthetic function. The serum ammonia level was normal. At 2 years of age, the patient exhibits marked developmental delay and is symptomatic of right heart failure.
Fig. 1a–e.

Patient 1. A 3-month-old girl with type 2 CEPS. a–c Contrast-enhanced magnetic resonance angiograms demonstrate interruption of the inferior vena cava with continuation to an enlarged azygos vein. A large aberrant shunt vessel (asterisks) drains the superior mesenteric (SMV) and splenic veins to the left renal vein. A tiny portal vein is visualized in c. d, e Axial spin echo T1- and T2-weighted and contrast-enhanced T1-weighted image through the upper abdomen. There are multiple left-sided spleens (Sp). There are three ill-defined lesions within the liver (numbers 1, 2 and 3). Lesions 1 and 2 are predominantly hyperintense to normal liver on T1 and hypointense on T2 images. Lesion 2 contains a central, contrast-enhancing focus that is consistent with a central scar or necrosis. These lesions probably represent focal nodular hyperplasia or regenerative nodules. Lesion 3 is relatively isointense to liver on T1 and hyperintense on T2 images with mild, homogeneous contrast enhancement. It is most likely a small hemangioma, adenoma or regenerative nodule

Patient 2

An 18-month-old girl presented with a 2-week history of rectal bleeding and peripheral edema secondary to hypoalbuminemia. The patient had been born at term with mild congestive heart failure. Echocardiography at that time revealed a perimembranous ventricular septal defect and a small atrial septal defect. Lower gastrointestinal endoscopy at the time of admission revealed rectal and colonic polyps and chromosomal analysis identified a balanced translocation 2,10 (q31; p15), with a provisional diagnosis of Bannayan-Riley-Ruvalcaba syndrome. Computed tomography and magnetic resonance imaging of the abdomen demonstrated the colorectal polyposis and a large shunt between the splenic vein and left renal vein. A portal vein was not identified on either modality. Magnetic resonance imaging showed a small nodular lesion in the right lobe of the liver (Fig. 2). The patient underwent a total colectomy that was complicated by Escherichia coli bacterial meningitis necessitating an extended intensive care unit admission; the patient was subsequently discharged without neurological sequelae. Liver function and biochemistry test results remained normal throughout the admission apart from the presence of hypoalbuminemia. At 2 years of age, the patient continues to experience rectal bleeding with anemia requiring intermittent red cell transfusions.
Fig. 2a–c.

Patient 2. An 18-month-old girl with type 1b CEPS. Axial spin echo T1- and T2-weighted and contrast-enhanced T1-weighted image through the upper abdomen. There is normal visceral situs. There is a small focus of increased T2 and slightly decreased T1 signal within the right lobe of the liver (arrow). This lesion demonstrates modest contrast enhancement and is consistent with either focal nodular hyperplasia or a regenerative nodule

Patient 3

A 4-year-old boy presented for follow-up postsurgical biliary diversion at 10 weeks of age for biliary atresia. Bowel malrotation and visceral situs ambiguous were suspected. Liver function tests demonstrated a mild elevation in transaminases and mildly elevated serum ammonia levels of 42 µg/dl (normal 0–34 µg/dl). The serum alpha fetoprotein level was normal. An abdominal ultrasound did not identify a portal vein and chronic portal vein thrombosis was suggested. Magnetic resonance imaging of the abdomen and heart revealed right-sided polysplenia and interruption of the inferior vena cava with azygos continuation on the right side. There were bilateral superior venae cavae. The mesenteric veins and splenic vein drained into the inferior vena cava through a fistulous connection to the right renal vein. A portal vein was not identified. The hemiazygos vein drained to the coronary sinus, as did a left-sided superior vena cava. In addition, two focal liver lesions were present (Fig. 3). Celiac angiography failed to demonstrate a patent portal vein. The patient underwent liver transplantation surgery and the smaller lesion was found to represent focal nodular hyperplasia. The larger lesion was difficult to characterize pathologically, but was considered to represent a fetal hepatoblastoma, with focal nodular hyperplasia or adenoma considered less likely. Portal veins and venules could be identified only at the histological examination of the explanted liver.
Fig. 3a–c.

Patient 3. A 4-year-old boy with type 2 CEPS. a Axial spin-echo T1-weighted image through the upper abdomen. There is polysplenia with multiple right-sided spleens (Sp) and interruption of the inferior vena cava with azygos continuation. There is a focus of altered signal intensity within the liver (arrow) representing focal nodular hyperplasia. b, c Axial spin echo T1- and T2-weighted images at a lower level than a demonstrate a second larger liver lesion (arrow) that is relatively isointense on T1- and mildly heterogeneous on T2-weighted images. It was considered to represent a hepatoblastoma histologically

Literature review

There have been 61 cases of CEPS reported in the literature to date (including our cases), 39 type 1 and 22 type 2 [1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38]. Type 1, and in particular type 1a, CEPS occurs predominantly in females (74% and 89%, respectively). The incidence of type 2 CEPS is essentially split between the sexes with 12 female and 10 male patients. The range of age at diagnosis for type 1 CEPS is 31 weeks of intrauterine life to 76 years, with a median age of 10 years. For type 2, the age varies from 28 weeks of intrauterine life to 69 years, with a median age of 18 months.

CEPSs are associated with other congenital anomalies, liver disease, and portosystemic encephalopathy. The more common associations, inclusive of the present data, are given in Table 3.
Table 3.

Associations of CEPS

Association

Type 1 (n=39)

Type 2 (n=22)

Total (n=61)

References

Congenital heart disease

13 (33%)

6 (27%)

19 (31%)

[1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15]

Focal nodular hyperplasia

11 (28%)

1 (5%)

12 (20%)

[2, 16, 17, 18, 19, 20, 21, 22, 23, 24]

Other nodular liver lesionsa

10 (26%)

3 (14%)

13 (21%)

[1, 2, 3, 5, 11, 13, 22, 23 25, 26, 27, 28c]

Portosystemic encephalopathy

7 (18%)

3 (14%)

10 (16%)

[8, 10, 14, 19, 20, 29, 30, 31]

Polysplenia

7 (18%)

2 (9%)

9 (15%)

[2, 3, 6, 10, 12, 17, 32c]

IVC interruption/azygos cont

3 (8%)

2 (9%)

5 (8%)

[23, 26, 34c]

Biliary atresia

6 (15%)

1 (5%)

7 (11%)

[3, 10, 12, 19, 32c]

Skeletal anomalies

4 (10%)

1 (5%)

5 (8%)

[9, 16b, 21, 25, 33b]

Renal tract anomalies

2 (5%)

2 (9%)

4 (7%)

[18, 21, 27, 35]

aIncludes hepatoblastoma, hepatocellular carcinoma, hepatic sarcoma, nodular regenerative hyperplasia, hyperplastic nodules, "likely" focal nodular hyperplasia, and other unclassified nodular liver lesions

bTwo patients had Goldenhar (oculoauriculovertebral dysplasia) syndrome

cPatients from this article

The clinical presentations of CEPS vary widely. Most often, shunts have been detected incidentally in the investigation of cardiac anomalies or liver dysfunction. Occasionally, shunts are detected as the cause of psychiatric disturbance or mental retardation secondary to chronic hyperammonemia. In CEPS there are typically no secondary signs of portal venous hypertension such as ascites, varices, or splenomegaly. A report in 1997 of a 5-month-old girl with type 1b CEPS has not been considered in the present literature review because of the presence of splenomegaly, possibly indicating portal hypertension [39].

Discussion

Development of the portal venous system occurs between the fourth and tenth weeks of embryonic life by selective apoptosis of portions of the left and right vitelline veins before they enter the septum transversum [40]. The development of the portal vein and inferior vena cava is a complex, coinciding process, which probably explains the potential for congenital portosystemic anastomoses. Shunting of mesenteric venous return to the inferior vena cava presumably leads to a marked diminution in flow within the normally developed portal venous system and therefore eventually to portal venous hypoplasia or atresia. Alternatively, hypoplasia or aplasia secondary to excessive involution of the vitelline venous system may be the initializing event [1, 2].

CEPS is most common to the inferior vena cava and less common to the renal veins, the iliac veins, the azygos vein, or the right atrium. Morgan and Superina [3] have classified CEPS into two types according to the presence or absence of the intrahepatic portal vein and further subclassified the first type into two groups depending on the status of the extrahepatic portal vein (Table 1).

CEPSs have been described in a variety of animals and are relatively common in dogs [41, 42]. CEPS may not be as rare in humans as is generally believed. In the reported cases, there was a significant female preponderance (74%) in type 1 CEPS, while female preponderance was not significant (54%) in type 2 [1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38]. Given the likelihood that some cases of type 2 CEPS have been misclassified as type 1, the true sex incidence for each type cannot be established. The younger median age for type 2 CEPS (2 years versus 10 years) contradicts the previously held belief that type 2 shunts are typically diagnosed in older children and adults [3].

To date, cases of congenital absence of the portal vein have generally been reported as a distinct entity. In congenital complete absence of the portal vein, a systemic shunt must be present and this therefore represents a type 1a CEPS. Strictly speaking, congenital absence of the portal vein is characterized by the lack of a junction between the superior mesenteric and splenic veins and independent outflow of these veins into the systemic circulation [3], as well as complete absence of venules within the portal triads at liver biopsy [38]. It is noteworthy that histological confirmation of the absence of hepatic portal venules has been made in only 8 of the 39 reported cases of type1 CEPS [5, 10, 20, 21, 23, 26, 37]. Of interest, Bellah et al. [4] described a patient in whom portal venous structures were not identified on ultrasound but later confirmed on liver biopsy. Yonemitsu et al. [5] reported a patient in whom portal venous structures were not identified on computed tomography, ultrasound, and liver biopsy, but were found on retrograde portography and computed tomography angioportography performed under balloon occlusion of the portocaval shunt. In patient 1 of the present series, a tiny portal vein was identified on magnetic resonance imaging. In patient 3, portal venules were only identified on histological examination of the explanted liver. On this basis, we propose that some of the previously described cases of type 1 CEPS may have actually been type 2, particularly those in which magnetic resonance imaging or X-ray angiography were not performed. In other words, intrahepatic portal venous flow may have been present but beyond the limits of resolution of the imaging available.

The importance of determining the type of shunt is heightened when considering candidacy for surgical ablation. Type 1 shunts should not be occluded as they represent the only drainage pathway for mesenteric venous return. However, work-up of the shunt should entail X-ray or magnetic resonance angiography so as not to exclude patients with diminutive intrahepatic portal systems from definitive treatment. Accurate preoperative depiction of the intra- and extrahepatic vascular anatomy will undoubtedly guide management decisions and the surgical or angiographic approach, to which end magnetic resonance imaging with contrast-enhanced angiography is recommended.

CEPSs are uncommon and under-recognized and as such no standard treatment is available. Children have generally been treated conservatively because of the associated abnormalities such as complex congenital heart disease or hepatobiliary dysfunction. Poor development of the intrahepatic portal veins is not considered a contraindication for definitive repair of the shunt [12, 14, 22]. Shinkai et al. [22] recently found that most patients with type 2 shunts can be treated with ligation or banding of the shunt vessel. In one case, Ikeda et al. [14] noted a return to almost normal size of the hypoplastic intrahepatic portal veins after coil embolization of a shunt. For patients with CEPS, early diagnosis and correction are needed to avoid the deleterious effects of hyperammonemia on the central nervous system [14].

CEPSs are often associated with nodular lesions of the liver, biliary atresia, skeletal anomalies, and renal tract anomalies (Table 3). The various associations of CEPS are consistently more common in type 1 with the exception of renal tract anomalies, which are evenly represented. Nevertheless, the coincidence of associations in both types suggests that the two variants are closely related.

Polysplenia with interruption of the inferior vena cava and azygos venous continuation was identified in patients 1 and 3 of our series representing a significant addition to the seven prior recorded cases of polysplenia and three recorded cases of interrupted inferior vena cava. There were possibly other cases of polysplenia and anomalous systemic venous drainage that were not specifically identified in the literature. The authors recommend screening for CEPS in patients diagnosed with polysplenia or anomalies of the abdominal systemic venous circulation.

Cardiac anomalies are a particularly common association with CEPS, having been recognized in patient 2 of the current article and nearly a third of cases overall. The most common lesion is an atrial septal defect. Coincidence of cardiac defects suggests either a prenatal insult during the simultaneous development of the heart and abdominal venous system, or an adaptive response to the hyperdynamic effect of CEPS [7, 11].

Nodular liver lesions are a fundamental response to almost any significant liver injury [43]. Nearly half of the recorded cases of CEPS describe associated nodular liver lesions. Focal nodular hyperplasia and other regenerative nodular lesions are associated with hepatic ischemia, and a compensatory increase in hepatic arterial flow is a possible stimulus [5]. Growth factors and hormones may also be important etiological factors [44]. Shinkai et al. [22] identified an association between small liver volumes and congenital absence of the portal vein, although this was not so in the present series. In focal nodular hyperplasia, the surrounding liver is histologically normal so that the stimulus to development of the nodule is probably not a decrease in functional liver mass [43]. Importantly, there is an association between CEPS and liver malignancy with case reports of hepatocellular carcinoma, hepatoblastoma, and sarcoma.

Biliary atresia is a disorder of unknown etiology that manifests as an inflammatory process involving the extrahepatic bile ducts in the late intrauterine or early neonatal period. Extrahepatic bile ducts appear from the intestinal bud at 5 weeks of embryonic life, therefore the association of biliary atresia with portal venous anomalies may indicate a shared insult in early development [32, 45]. Of 61 cases, seven (11%) were associated with biliary atresia and all but one of these was type 1. Of the seven cases associated with biliary atresia, five (71%) also had polysplenia, reiterating the known association of biliary atresia and the polysplenia syndrome and again suggesting a common insult in early fetal life [46].

Toxic compounds produced in the digestion process are normally metabolized in the liver. CEPSs cause some or all of the mesenteric circulation to bypass the liver, delaying the metabolism of galactose and ammonia, amongst other potentially dangerous metabolites. Newborn screening for high blood galactose levels has recently been found to be useful for the detection of congenital portosystemic shunts. Portosystemic encephalopathy was previously considered a rare association of CEPS, although careful review of the literature indicates that 16% of cases showed encephalopathy [2, 3, 10,15]. It is generally believed that portosystemic encephalopathy may manifest later in life as the younger brains are less sensitive to toxic materials; however, seven of the ten reported cases were children [14].

Conclusion

CEPS is a rare though increasingly reported anomaly that is important to diagnose given the potentially dire clinical consequences. CEPSs have several associations that the radiologist should be aware of, in particular the association with polysplenia, nodular lesions of the liver including malignancy, congenital heart disease, and hepatic encephalopathy. It is important to identify the presence or absence of hepatic portal venous supply as this may influence treatment options. Magnetic resonance imaging is recommended as a noninvasive imaging technique for the identification and classification of CEPS with the aim of guiding management and improving outcomes.

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© Springer-Verlag 2003