- Open Access
Spectrum of hepatofugal collateral pathways in portal hypertension: an illustrated radiological review
© The Author(s) 2015
- Received: 7 May 2015
- Accepted: 29 June 2015
- Published: 4 September 2015
The purpose of this article is to describe the various portosystemic collateral pathways pertinent to portal hypertension on multi-detector row computed tomography (MDCT) and their clinical relevance, with special emphasis on the uncommon ones. The knowledge and understanding of the various patterns of portosystemic collateral channels has important implications both for the clinician and the interventionist. MDCT with its advanced post processing capabilities can exquisitely demonstrate these vascular pathways to help in therapeutic decision making.
• Portosystemic collaterals are an important cause of bleeding and hepatic encephalopathy.
• Radiologists should be familiar with the imaging findings to effectively identify them.
• Pre-operative knowledge of portosystemic collaterals is essential to avoid inadvertent vascular injury.
- Collateral pathways
- Multi-detector row computed tomography
- Portal hypertension
Portal hypertension (PHTN), characterized by a pathological increase in the portal venous pressure, is one of the key consequences of liver cirrhosis . It results from a combination of increased intrahepatic vascular resistance and augmented blood flow through the portal venous system . This high-pressure hepatopetal flow is redirected through alternative pathways into the low-pressure systemic veins, leading to formation of an extensive network of portosystemic collateral vessels (PSCV) . Detection of these ‘spontaneous’ PSCV serves as an important tool in diagnosing portal hypertension and predicting prognosis . The radiological appearances of the common PSCV, including gastro-oesophageal and para-oesophageal collaterals, gastrorenal or splenorenal shunts, and paraumbilical shunts have been studied at length [4–8]. However, with the advent of multi-detector row computed tomography (CT), unusual pathways of portosystemic anastomoses are increasingly being recognized, yet have not been well described in the literature [9–14]. Since these shunts could be an important cause of variceal bleeding and hepatic encephalopathy, their accurate identification is imperative in therapeutic decision making. In addition, understanding their anatomy may help to avoid potential complications related to interventional radiological procedures and surgery. The purpose of this review is to appraise the spectrum of common and uncommon collateral pathways of the portal venous system that can be encountered in PHTN at CT examinations.
Normal sites of portosystemic anastomoses
Left gastric vein
Rectum and anal canal
Superior rectal vein
Middle and inferior rectal veins
Superior and inferior epigastric veins
Bare area of liver
Portal venous branches
Inferior phrenic and right internal thoracic vein
Tributaries of splenic and pancreatic and colic veins
Renal, suprarenal, paravertebral and gonadal vein
Patent ductus venosus (rare)
Left branch of portal vein
Inferior vena cava (IVC)
In PHTN, dilatation of these channels leads to formation of varices at various sites in the body, which are mostly classified into two groups, the gastro-oesophageal varices and ectopic varices  (Fig. 1). These varices are fed in the long term by spontaneous development of large shunts in the abdomen, which can be anatomically divided into intrahepatic, transhepatic and extrahepatic shunts [9–12] (Fig. 1).
Oesophageal and para-oesophageal varices
Oesophageal varices are the most common to bleed in cirrhotic patients, owing to the high-volume of blood carried by them, and account for the high mortality associated with spontaneous variceal bleeding .
Gastric and perigastric varices
The risk of bleeding from gastric varices is known to be lower than that from oesophageal varices, however, the severity of bleeding and the associated mortality is significantly higher, because of their large size and rapid blood flow . Various treatment modalities, such as pharmacotherapy, balloon tamponade, endoscopic procedures, endovascular treatment, and surgery, have been used in their management [24–26]. For patients in whom endoscopic therapy fails to control the GV bleed or who re-bleed, interventional radiological techniques such as transjugular intrahepatic portosystemic shunt (TIPS), balloon-occluded retrograde obliteration of varices (B-RTO) or percutaneous transvenous embolisation (PTVE) of varices can be done [20, 23, 25]. In majority of the cases, the anatomy of varices dictates the approach used for treatment. Familiarity with the afferent and efferent veins is of paramount importance, as the degree of difficulty in performing endovascular obliteration of gastric varices and the success of the procedure are directly correlated with the anatomic complexity of the varix .
Ectopic varices account for 2–5 % of gastrointestinal tract variceal bleeding [27–29]. However, they have a fourfold increased risk of bleeding when compared with oesophageal varices, and can have a mortality rate as high as 40 % [28–32].
Ectopic varices can either be a result of global portal hypertension or splanchnic venous occlusion. These occlusions can be due to thrombosis of the main portal vein, splenic vein, mesenteric veins or of a spontaneous gastrorenal shunt (post B-RTO) . The occlusion can also be due to postoperative adhesions, scarring, and postoperative-altered anatomy [27, 31].
The standard management of ectopic varices has not yet been established. However, it is known that when bleeding occurs from ectopic varices, it is difficult to control by any means, and the bleeding is potentially fatal. All treatment strategies and techniques have been utilised in their management, including medical (systemic vasopressin and octreotide) and endoscopic therapy (banding/ligation and injection therapy), decompression using TIPS and partial splenic artery embolisation, antegrade/retrograde obliteration and surgical ligation [27–30, 32–35]. However, all of them have shown poor outcomes, underlining the importance of early diagnosis and therapy of these varices. Better understanding of ectopic varices is needed for a more systemic approach to this rare but menacing problem.
The afferent vessel can be formed by any of the tributaries of portal venous system and commonly include the superior and inferior pancreaticoduodenal veins, cystic branches of the superior mesenteric veins, gastroduodenal vein, and pyloric vein [3, 7]. The efferents flow hepatofugally via retroperitoneal shunts (also called veins of Retzius) into the IVC via the right gonadal veins (mesenterico-gonadal shunt) or the capsular renal veins (mesenterico-renal shunt) [3, 7].
Bronchial varices are speculated to develop through collateral channels which normally exist between the tracheal and oesophageal venous systems . There have been only three case reports in English-language medical literature describing bronchial varices secondary to portal hypertension [45–47]. Two of these were in patients with alcoholic liver cirrhosis and oesophageal varices [46, 47], while the third was secondary to extrahepatic portal vein stenosis . All the previously reported cases presented with hemoptysis. In one of them, the bleeding was massive and required portosystemic shunting and embolisation .
Mesenteric collateral vessels may arise from the superior mesenteric vein (SMV) and inferior mesenteric vein (IMV) and ultimately drain into the IVC via the retroperitoneal or pelvic veins (also called the veins of Retzius) [48, 49]. In contrast to other portosystemic shunts, the veins of Retzius are often not dilated even in patients with portal hypertension, and hence are not well recognized. Various pathways of veins of Retzius are defined according to the receiving vein (mesenterico-gonadal/renal/caval or iliac)
Anastomotic and stomal varices
In the setting of chronic portal vein thrombus, collaterisation usually occurs through the hepaticoduodenal ligament, resulting in the formation of a portal cavernoma. However, in patients who have undergone previous hepatobiliary surgery, formation of the classical portal cavernoma can be precluded by the surgical dissection of preformed primitive vascular structures in the hepatoduodenal ligament . In these patients, collateral channels can develop at unusual locations. Previously described entities include porto-portal varices in patients with enteroenteric anastomosis  and dilated communicating channels between jejunal veins and intrahepatic portal vein branches in patients with hepaticojejunostomy .
Rectal and perirectal varices
For a surgeon considering an anorectal surgery, these collaterals are of special clinical concern, because an anorectal anastomosis through the inferior mesenteric vein can potentially cause catastrophic haemorrhoidal bleeding.
Accessory portal veins described by Sappey
Upper part of falciform ligament
Superior veins of Sappey
Lower part of falciform ligament
Inferior veins of Sappey
Bare area of liver
Left triangular ligament
Left inferior phrenic vein and intercostal vein
Right triangular ligament
Right inferior phrenic vein
Cystic veins and branches of LGV
Recanalised paraumbilical vein
In the presence of prominent anterior abdominal wall collaterals, a seemingly innocuous procedure like paracentesis could cause serious complications, if done without imaging guidance. Similarly, in the presence of abdominal wall or paraumbilical collaterals, even a simple hernia operation can become a dreaded procedure. Even with knowledge of a recanalised paraumbilical vein, the true extent and complexity may be underestimated without explicit information about its course and size. More recently, recanalised paraumbilical vein has been used as an access route for percutaneous embolisation of bleeding gastro-oesophageal and umbilical varices [60, 61].
Right infradiaphragmatic shunt/ apex type shunt
In the right infradiaphragmatic shunt, the collateral vein arising from a peripheral branch of left portal vein drains into the internal thoracic vein and the intercostal vein [10, 11]. This vein is also called the superior vein of Sappey . The hepatofugal blood directed through this shunt into the internal thoracic vein reaches the right heart via the brachiocephalic vein and the SVC. In patients with SVC syndrome, contrast medium or isotopes injected into the arm go into the liver through this shunt, explaining the “hot” spot that is sometimes shown in the liver of these patients [10, 62].
Left infradiaphragmatic shunt/left triangular ligament shunt
Right posterior portal branch-inferior vena cava (IVC) shunt
Dilated collateral vessel arising from the right posterior portal vein runs across the posterior surface of the liver, forms a venous aneurysm outside the liver, and drains into the IVC directly or through the adrenal vein [10–12].
Bare area shunt
Aberrant left gastric vein draining into the left portal vein
This refers to a communication between the main portal and the azygos veins. While congenital portoazygos shunts have been extensively described in certain dog breeds , it is rare in humans, with only a single case report describing this entity in a neonate with thoraco-abdominal duplication and absent intrahepatic portal vein . Its description in association with liver cirrhosis and portal hypertension is also limited to a solitary case report. In this report, the shunt was seen between the posterior aspect of the main portal vein and the azygos vein along the right aspect of the thoracolumbar vertebrae . It may be asymptomatic, but can cause hepatic encephalopathy or variceal bleeding. Treatment options include endovascular transvenous coil embolisation or surgical ligation .
Gastrorenal and splenorenal shunts
Direct splenorenal shunts constitute a direct communication between the splenic vein and the left renal vein, sometimes through the splenic capsule. This type of direct portosytemic shunting is similar to the direct shunting of blood from posterior branch of the left gastric vein to para-oesophageal veins and azygos vein without formation of oesophageal varices.
Large spleno/gastro-renal shunts are often found in patients with recurrent or chronic hepatic encephalopathy, and B-RTOof these has shown good results in improving the patient’s neurological status [25, 65].
Coronary/splenic-inferior pulmonary/inferior phrenic/intercostal veins
The left gastric vein or splenic vein communicates with the inferior pulmonary vein, pericardiophrenic vein or to intercostal vein .
PSCV developing in the setting of Budd-Chiari syndrome and extrahepatic portal venous obstruction are a separate topic and have not been discussed here.
Unusual portosystemic collateral pathways are increasingly being encountered in the daily clinical practice. Since these could be an important cause of bleeding and hepatic encephalopathy, radiologists should be familiar with the imaging findings to effectively identify them and aid in therapeutic decision making. Also, pre-operative knowledge of the anatomy and course of these uncommon portosystemiccollaterals is essential for interventional radiologists and surgeons to avoid inadvertent vascular injury during the procedures.
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