Assessment of surgical portosystemic shunts and associated complications: The diagnostic and therapeutic role of radiologists.

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European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad

Assessment of surgical portosystemic shunts and associated complications: The diagnostic and therapeutic role of radiologists Bedros Taslakian a , Walid Faraj b , Mohammad Khalife b , Aghiad Al-Kutoubi a , Fadi El-Merhi a , Charbel Saade a , Ali Hallal b , Ali Haydar a,∗ a b

Department of Radiology, American University of Beirut Medical Center, Riad El-Solh 1107 2020—PO Box: 11-0236, Beirut, Lebanon Department of General Surgery, American University of Beirut Medical Center, Riad El-Solh 1107 2020—PO Box: 11-0236, Beirut, Lebanon

a r t i c l e

i n f o

Article history: Received 24 February 2015 Received in revised form 16 April 2015 Accepted 21 April 2015 Keywords: Budd–Chiari syndrome Portal hypertension Surgical portosystemic shunt Imaging Interventional radiology Portosystemic shunt

a b s t r a c t Surgical portosystemic shunting, the formation of a vascular connection between the portal and systemic venous circulation, has been used as a treatment to reduce portal venous pressure. Although the use of portosystemic shunt surgery in the management of portal hypertension has declined during the past decade in favour of alternative therapies, and subsequently surgeons and radiologists became less familiar with the procedure, it remains a well-established treatment. Knowledge of different types of surgical portosystemic shunts, their pathophysiology and complications will help radiologists improve communication with surgeons and enhance their understanding of the diagnostic and therapeutic role of radiology in the assessment and management of these shunts. Optimal assessment of the shunt is essential to determine its patency and allow timely intervention. Both non-invasive and invasive imaging modalities complement each other in the evaluation of surgical portosystemic shunts. Interventional radiology plays an important role in the management of complications, such as shunt thrombosis and stenosis. This article describes the various types of surgical portosystemic shunts, explains the anatomy and pathophysiology of these shunts, illustrates the pearls and pitfalls of different imaging modalities in the assessment of these shunts and demonstrates the role of radiologists in the interventional management of complications. © 2015 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Portal hypertension is defined as the pathological increase in portal venous pressure in which the pressure gradient is increased above the upper normal limit of 5 mmHg. [1,2]. Common causes of noncirrhotic portal hypertension include Budd–Chiari syndrome, veno-occlusive disease, extrahepatic portal vein obstruction (EHPVO), schistosomiasis, noncirrhotic portal fibrosis, idiopathic portal hypertension and congenital hepatic

Abbreviations: CT, computed tomography; EHPVO, extrahepatic portal vein obstruction; IVC, inferior vena cava; MIP, maximal intensity projection; MPR, multiplanar reconstruction; MRA, magnetic resonance angiography; MRI, magnetic resonance imaging; SPSS, surgical portosystemic shunt; SSSR, side-to-side splenorenal; TIPS, transjugular intrahepatic portosystemic shunt; US, ultrasound; VR, volume-rendered reconstruction. ∗ Corresponding author. Tel.: +961 1 350 000x5020; fax: +961 1 743634. E-mail addresses: [email protected] (B. Taslakian), [email protected] (W. Faraj), [email protected] (M. Khalife), [email protected] (A. Al-Kutoubi), [email protected] (F. El-Merhi), [email protected] (C. Saade), [email protected] (A. Hallal), [email protected] (A. Haydar).

fibrosis [3,4]. Most types of noncirrhotic portal hypertension have preserved liver function even in advanced stages of the disease, thus hepatic decompensation is rare and liver transplantation is seldom indicated [3,4]. Variceal bleeding, ascites, hepatorenal syndrome, spontaneous bacterial peritonitis, hepatic encephalopathy and sequelae of hypersplenism are known complications of portal hypertension [2,4]. The available therapies for portal hypertension are diverse, and factors that influence the prognosis should be considered when stratifying risks and selecting a therapy. Thus, different stages of portal hypertension require tailored management, including supportive medical and/or endoscopic treatment, surgical portosystemic shunt (SPSS) creation, transjugular intrahepatic portosystemic shunt (TIPS) or liver transplantation [2]. The selection of a specific treatment method is determined by whether the predominant manifestation is liver failure or portal hypertension. It also depends on the potential for parenchymal recovery, the surgical risk, and the availability of a liver donor. SPSS is one of the accepted methods of treatment for refractory gastrointestinal haemorrhage due to portal hypertension [5,6]. It is the formation of a vascular connection between the portal venous circulation (superior mesenteric, portal or splenic vein) and

http://dx.doi.org/10.1016/j.ejrad.2015.04.021 0720-048X/© 2015 Elsevier Ireland Ltd. All rights reserved.

Please cite this article in press as: Taslakian B, et al. Assessment of surgical portosystemic shunts and associated complications: The diagnostic and therapeutic role of radiologists. Eur J Radiol (2015), http://dx.doi.org/10.1016/j.ejrad.2015.04.021

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Fig. 1. Schematics showing types of non-selective portosystemic shunts: [a] Side-to-side portocaval shunt. [b] H-type interposition portocaval graft. [c] H-type interposition mesocaval graft. [d] Side-to-side mesocaval shunt. [e] Portoatrial shunt. [f] Mesoatrial shunt. [g] Mesoinnominate shunt [IVC = asterisk, superior mesenteric vein = open arrow, portal vein = arrow, right atrium = RA, right innominate vein = curved arrow, graft/anastomosis = double arrow].

systemic venous circulation (inferior vena cava, right atrium, right innominate vein or left renal vein) to decompress the liver using the portal venous system as an outflow tract and the systemic venous system as an inflow tract. The use of SPPS to lower portal hypertension and decompress bleeding gastro-oesophageal varices has declined during the past decade in favour of alternative therapies, such as medical and endoscopic management, TIPS and liver transplantation [4,5]. TIPS has largely replaced surgical shunts, therefore experience with the surgical procedure and interpretation of imaging studies is declining. Furthermore, SPSS creation has a significant risk, when compared to interventional management which has lower rates of morbidity and mortality [7]. In the rare instance when a surgical shunt is necessary, the possibility of future liver transplantation has to be considered. The presence of a SPSS, especially when a direct connection with the portal vein is created, complicates liver transplantation and may increase intraoperative blood loss and perioperative mortality [8,9]. This articles provides a comprehensive review of the different types of SPSSs, their pathophysiology and potential complications. We describe the role and limitations of each imaging modality in the assessment of SPSSs and discuss the role of radiologists in the diagnosis and management of complications.

2. Indications of surgical portosystemic shunts The main indication for SPSS creation is to lower portal hypertension and decompress bleeding gastro-oesophageal varices after failure of medical and endoscopic treatment. Other indications include the presence of isolated gastric varices, portal hypertensive bilopathy, small for size syndrome in liver transplantation and contraindications to, or re-bleeding after, TIPS [10–12]. Familial hypercholesterolemia is another indication for SPSS in children and proved to be effective in reducing hepatic synthesis of both cholesterol and lipoproteins, although liver transplantation is now the treatment of choice [6,13].

3. Types of surgical portosystemic shunts Surgical portosystemic shunts are divided into two categories (Table 1) based on complete or partial diversion of the splanchnic venous flow [6]: Non-selective SPSSs (Fig. 1) are designed to decompress the portal venous circulation with complete diversion of portal blood flow from the liver into the systemic circulation. On the other hand, selective SPSSs (Fig. 2) serve to decompress gastro-oesophageal varices through the short gastric and splenic




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Fig. 3. Intra-operative image of a side-to-side portosystemic shunt, showing the surgical anastomosis at the level of the clamp. [IVC = asterisk, portal vein = arrow].

Fig. 2. Schematics showing types of selective portosystemic shunts: [a] Sideto-side spleen preserving splenorenal shunt. [b] End-to-side splenorenal shunt with splenectomy. [IVC = asterisk, superior mesenteric vein = open arrow, portal vein = arrow, splenic vein = dotted arrow, left renal vein = arrowhead, splenorenal anastomosis = double arrow].

veins to the left renal vein, maintaining the superior mesenteric and portal vein flow to the liver [14,15]. SPSSs can be created by either direct side-to-side (Fig. 3) or end-to-side anastomosis, or by using a synthetic or autologous vein interposition graft [16,17].

Fig. 4. Patent side-to-side portocaval shunt in a 21 year-old male with Budd–Chiari syndrome. [a] Axial T2-weighted MRI of the abdomen showing the flow void in the IVC and at the anastomosis. [b] Axial T1-weighted fat suppressed MRI after gadolinium administration [MIP-25 mm thickness] and [c] axial enhanced CT of the abdomen [MIP-25 mm] showing a patent shunt. [IVC = asterisk, portal vein = arrow, anastomosis = double arrow].




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Fig. 5. Patent side-to-side mesocaval shunt created after unsuccessful attempt to catheterize an occluded mesocaval interposition graft in a 17 year-old female with Budd–Chiari-Syndrome due to isolated hepatic vein occlusion. [a] Axial contrast-enhanced CT [MIP-20 mm thickness] image showing a patent mesocaval shunt. [b] Coronal and [c] sagittal oblique multiplanar reconstruction showing the thrombosed mesocaval graft with non-opacification of the graft lumen, and patent side-to-side mesocaval anastomosis. [d] Volume rendering reconstruction from the CT scan showing the mesocaval graft and delineating the vascular anatomy. [IVC = asterisk, superior mesenteric vein = open arrow, side-to-side anastomosis = black double arrow, mesocaval graft = white double arrow].

3.1. Non-selective shunts Non-selective shunts are simpler to construct, but their use in patients with advanced liver disease is complicated by a high incidence of hepatic encephalopathy when compared to selective shunts [18]. In patients with portal hypertension resulting in liver dysfunction, elective surgical decompression using portal flow preserving techniques such as a selective distal splenorenal shunt or a partial portal decompression using a small diameter interposition portocaval graft is preferred, with the advantage of decreasing the occurrence of post-shunting encephalopathy [18,19]. In emergency cases, TIPS has become one of the preferred methods of portal decompression to control variceal bleeding, with the endto-side portocaval shunt serving as a salvage procedure if both emergency endoscopic treatment or TIPS insertion fails to stop bleeding [3]. The mesocaval interposition graft gained popularity due to its technical simplicity; insertion can be rapidly performed and is associated with minimal blood loss [20,21]. Interposition of the shunt does not require extensive vein mobilization or dissection, and the graft can easily be taken down should the decision be made to proceed to liver transplantation [9,20,21]. In a good-prognosis subgroup of patients with Budd–Chiari syndrome, a side-to-side portocaval shunt (Fig. 4) or a mesocaval interposition graft (Fig. 5) can establish an adequate portal outflow tract to decompress the congested liver. Mesocaval shunt is also

considered the preferred shunt in the setting of isolated hepatic vein thrombosis in many studies [22,23]. The synthetic interposition grafts have a higher incidence of thrombosis and lower long-term patency rate [16]. In Budd–Chiari syndrome, depending on the patency of the inferior vena ava (IVC) and on technical limitations related to caudate lobe enlargement and secondary compression of the IVC, several variants of surgical shunting have been used, such as portoatrial, mesoatrial and mesoinnominate shunts [24–26]. A combination of mesocaval or portocaval shunts with IVC bypass (cavoatrial shunt) or IVC stenting (Fig. 6) have been used to overcome the compression of IVC by caudate lobe enlargement [16,27,28]. 3.2. Selective shunts End-to-side splenorenal shunt with splenectomy (Fig. 7) was one of the earliest used shunts [29]. However, because of its many side effects, particularly post-splenectomy sepsis [29], it has fallen from preference and other types of splenorenal shunts have been proposed. In symptomatic noncirrhotic portal hypertension with a patent portal system, surgical spleen-preserving side-to-side splenorenal (SSSR) shunts are the preferred type of therapy because of the good prognosis of the disease, low risk of encephalopathy and post-splenectomy sepsis, and durable decompression providing excellent quality of life, especially in pediatric patients [4].




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Table 1 Types of surgical portosystemic shunts. SPSS

Type

Description & surgical technique

Comments

Non-selective

Portocaval (Fig. 1a and b)

Shunt connecting the PV with the IVC Side-to side anastomosis or using a conduit Shunt connecting the SMV with the IVC Side-to side anastomosis or using a conduit Shunt connecting the PV with the RA using a long conduit Shunt connecting the SMV with the RA using a long conduit Shunt connecting the SMV with the right innominate vein using a long conduit Shunt connecting the distal splenic vein with left renal vein, without splenectomy Side-to side anastomosis Shunt connecting the distal end of the splenic vein after splenectomy with the left renal vein End-to-side anastomosis

Higher rate of encephalopathy compared to selective shunts

Mesocaval (Fig. 1c and d) Portoatrial (Fig. 1e) Mesoatrial (Fig. 1f) Mesoinnominate (Fig. 1g) Selective

Distal spleen-preserving splenorenal (Fig. 2a) End-to-side splenorenal (Fig. 2b)

Performed in patients with Budd–Chiari syndrome and IVC occlusion Higher rate of graft occlusion Lower risk for encephalopathy and post-splenectomy sepsis Lower risk for encephalopathy High risk for post-splenectomy sepsis

IVC = inferior vena cava, PV = portal vein, RA = right atrium, SMV = superior mesenteric vein.

Fig. 6. [a] Axial enhanced CT and [b] sagittal multiplanar reconstruction showing a patent opacified IVC stent [right-angled arrow] and portocaval H-graft [double arrow] in a patient with Budd–Chiari syndrome.

Spleen-preserving SSSR shunt was first described by Cooley, as a method of overcoming the high rates of encephalopathy seen after construction of non-selective shunts in patients with portal hypertension and advanced liver disease [30], and has a reported excellent long-term patency rate and low incidence of recurrent bleeding [5]. The SSSR shunt also reduces the size of the spleen, reversing hypersplenism, and does not interfere with subsequent liver transplantation [5]. The SSSR shunt is also preferred in adult patients with EHPVO, in view of its technical ease and low incidence

Fig. 7. End-to-side splenorenal shunt after splenectomy in a 51 year-old female with portal hypertension due to portal vein thrombosis. [a] Coronal oblique CT portography [MIP- slide thickness 18 mm] image showing a patent shunt, with dilated left renal and splenic veins. [b] Volume rendered reconstruction provides a global 3-dimentional view of the shunt and relevant vascular structures. [Left renal vein= arrowhead, splenic vein = dotted arrow, superior mesenteric vein = open arrow, left kidney = Kd].

of portosystemic encephalopathy [5]. In addition, as thrombosis of the portal vein is frequently the cause of EHPVO, the portal vein can rarely be used to construct a shunt. However, the management pattern for EHPVO, especially in children, has changed over the past decade after the introduction of the mesoportal




Fig. 9. H-type portocaval graft in a 23 year-old female patient with Budd–Chiari syndrome presenting with new onset of ascites 3 months after surgery. Cavograms before [a] and after [b] IVC stenting show mild narrowing of the IVC [asterisk] due to compression by the caudate lobe resulting in shunt dysfunction. IVC stenting improved the shunt function, with resolution of symptoms.

Fig. 8. [a] Enhanced coronal CT of the abdomen, with the contrast injected through a pedal vein and [b] corresponding volume rendering reconstruction, in a patient presenting with worsening jaundice and abdominal distension. Images show new onset ascites, thrombosed IVC stent [right-angled arrow] and a kinked thrombosed portocaval stent [double arrow]. Note the opacified infra-hepatic IVC [asterisk] and azygos vein [arrowhead] which is filling through the regular connection [curved arrows] descending through the aortic hiatus and terminating into the dorsal aspect of the IVC at the level of the renal veins.

bypass, which can restore physiological hepatic circulation with subsequent metabolic benefits when compared to SPSS [31]. Therefore, the mesoportal shunt, a surgical bypass connecting the superior mesenteric vein to the left portal vein, is theoretically the best option for patients with EHPVO and a patent left portal vein, because it maintains physiological portal flow through the liver [32]. This type of shunts is however beyond the scope of our discussion. 4. Complications of portosystemic shunts Successful shunt surgery achieves relief of portal hypertension and correction of most of its complications. Early post-operative complications include bleeding, seroma, abscess, encephalopathy, graft infection and thrombosis. There are potential

long-term complications that have been reported in patients with SPSSs. The most significant of these complications include shunt thrombosis, an increased surgical risk during subsequent liver transplantation, development of liver nodules, and portosystemic encephalopathy. Shunt thrombosis is a serious complication, more frequently encountered when using a conduit, and can be related to technical problems, such as graft compression and kinking (Fig. 8), or a hypercoagulable state in patients with Budd–Chiari syndrome. SPSS thrombosis usually presents with recurrent variceal hemorrhage and ascites, or signs and symptoms of obstructive jaundice [33]. Variceal hemorrhage following SPSS occlusion can be life-threatening [34]. In cases of shunt thrombosis, the shunt may be salvageable either by surgical revision, or by radiological intervention through percutaneous recanalization and/or balloon angioplasty [35]. Shunts connecting with the right atrium or the innominate vein are associated with a higher rate of postoperative thrombosis most likely because of the long prosthetic graft. In addition, shunt dysfunction and thrombosis might be secondary to IVC compression by the enlarged caudate lobe, decreasing the flow in the shunt towards the systemic venous outflow tract (Fig. 9). Encephalopathy is a frequent problem after conventional shunt surgery in patients with cirrhosis, but occurs infrequently in those without parenchymal disease [35]. Patients with cirrhosis are




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Table 2 The complementary role of different imaging modalities in the assessment of SPSSs. Ultrasound Main applications

Advantages Disadvantages Suggested technique Signs of patency

Signs of dysfunction

Magnetic resonance imaging Main applications Advantages Disadvantages Suggested technique

Signs of patency Signs of dysfunction Computed tomography Main applications Advantages Disadvantages Suggested technique

Signs of patency Signs of dysfunction Conventional angiography Main applications Advantages Disadvantages Suggested technique Signs of patency Signs of dysfunction

Primary modality of choice for post-operative assessment and follow-up Assessment method of intrahepatic portal blood flow hemodynamics Difficult to perform for the assessment of shunts located deep in the abdomen (e.g. splenorenal, mesoatrial) Inexpensive modality, performed by the bed-side; no exposure to radiation or need of contrast material administration; provides physiologic data Depends on the SPPS location and presence of acoustic window; operator dependent; difficult to image anastomosis Real time US for anatomical imaging Doppler US for flow imaging Direct signs: absence of post-stenotic jet; detection of color-coded flow within the shunted splanchnic vein, the shunt and systemic vein; appropriate flow direction Indirect signs: hepatofugal flow in the intrahepatic portal veins after surgery; decrease in the diameter of collateral vessels; decrease in the size of the spleen and amount of ascites Direct signs: absence of color-coded flow in the shunt indicating occlusion; flow velocity >190 cm/s or 50 cm/s) compared with the prior examination indicating shunt dysfunction Indirect signs: recurrent ascites, gastrointestinal bleeding; increase in the diameter of or formation of new portosystemic collateral vessels; increase in the size of spleen Imaging of deep shunts in different orientations Assessment of enhancement pattern of liver parenchyma and detection of hepatic lesions Reliable non-invasive modality; provides anatomical information on abdominal organs and vasculature; multiplanar image acquisition; can be performed in patients with renal dysfunction using time-of-flight MRA without the need of contrast administration Expensive; challenging in critical patients; artifact from coils/surgical clips/motion/ascites; limited spatial resolution Anatomical imaging; dynamic gadolinium enhanced imaging; time-of-flight angiographic technique Portal venous phase imaging is performed following 45 s delay from the initiation of contrast injection for infants and small children, and 65 s for adults Presence of low signal “flow void” on T2-weighted images; contrast opacification on multiphasic gadolinium enhanced sequences; presence of flow on time-of-flight MRA High signal intensity on T2-weighted images, absence of contrast opacification on multiphasic gadolinium enhanced sequences; absence of flow on time-of-flight MRA Imaging of deep shunts in different orientations using reconstruction techniques Assessment of enhancement pattern of liver parenchyma and detection of hepatic lesions High spatial resolution; relatively minimally invasive; reconstruction technology available Exposure to radiation and use of contrast material Multiphasic contrast enhanced imaging, with portal venous phase best obtained following a delay of approximately 45 s from the initiation of nonionic contrast injection (3 mL/kg; maximum 150 mL) for children and 60–65 s for adults using power injector at a rate of 2–3 mL/s Contrast opacification of the shunt; absence of signs of increased portal pressure (ascites, splenomegaly, collateral circulation) Absence of contrast opacification of the shunt indicating thrombosis/occlusion; narrowing at anastomosis; development of signs of portal hypertension (increase in ascites, splenomegaly, collateral circulation) Confirmation and interventional management of shunt dysfunction or occlusion Pressure measurement Gold standard; allows recanalization of stenotic or occluded shunts Expensive; invasive; exposure to radiation; use of contrast material Splenoportography (rarely used); indirect arterial portography; direct catheterization of the shunt and shuntography Presence of flow in the shunt towards the systemic circulation Absence of appropriately directed flow in the shunt towards the systemic circulation

likely to develop postoperative hepatic encephalopathy after creation of non-selective portosystemic shunts, which completely divert portal blood flow away from the liver and results in loss of the hepatopedal portal blood flow [36]. Chronic portosystemic encephalopathy, which may develop after shunt surgery and can be refractory to medical management, is a devastating clinical problem that impairs life and leads to permanent neurological deficit [37]. Liver nodules, such as liver cell adenomas, focal nodular hyperplasia and regenerative nodules may develop in the long term in some patients after SPSS, but the risk appears to be low. They are seen mostly in those patients with prolonged survival who have not required transplantation; therefore long term ultrasound screening is suggested [38]. Indirect signs indicating SPPS dysfunction arise from the consequences of increased portal venous pressure, such as increase in the size of the spleen, new or recurrent ascites, and increase in the size of or development of new spontaneous portosystemic collaterals.

5. Role of imaging in the assessment of portosystemic shunts Imaging plays a pivotal role to determine patency and detect complications of the SPSSs. Utilization of various imaging modalities allows detection of portal vein or IVC thrombosis and the visualization of the resultant changes in liver morphology and enhancement patterns, venous collaterals, varices, and ascites. Both non-invasive and invasive imaging modalities complement each other in the evaluation of portosystemic shunts (Table 2). Different noninvasive techniques are used in the assessment of SPPSs, including real time ultrasound (US) [39], color and duplex Doppler US [40–42], magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) [43], and contrast-enhanced computed tomography (CT) [44,45]. The patency of surgical portosystemic shunts can be assessed by invasive techniques such as arterioportography, indirect arterial portography and selective trans-anastomotic phlebography.




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Fig. 10. Color Doppler images of the [a] portocaval graft [double arrow] and [b] the stented IVC [right-angled arrow], showing internal color-coded signal indicating patency in a patient presenting with signs and symptoms of shunt dysfunction. [c] Spectral Doppler image of the portocaval graft showing a flow velocity of 39.3 cm/s. Note the presence of new onset ascites.

5.1. Ultrasound Sonography is an established noninvasive method for evaluation of SPSSs. Real-time US provides anatomical images that can suggest patency, using indirect signs such as decrease in the diameter of spontaneous portosystemic collateral vessels and absence of signs of portal hypertension (splenomegaly, ascites, and thickened lesser omentum) [46]. Doppler US provides physiologic flow information and has been successfully used in the assessment of SPSS as the primary investigation tool [40,42]. It can accurately demonstrate shunt patency [40,42], with a reported sensitivity and specificity of 100% [40,47]. It can be performed by the bed-side in critical patients with no exposure to ionizing radiation or need for contrast administration [40,48]. It is a reliable assessment method of the hemodynamic changes in intrahepatic portal venous blood flow after surgery, which depends on the SPSS type [42]. However, ultrasound imaging is operator dependent and sometimes difficult, because it depends on the location of the shunt and presence of an acoustic window for good visualization of the shunt [40]. Spectral Doppler imaging can be unsuccessful if real-time visualization of the shunt is insufficient to allow accurate placement of the Doppler cursor, particularly when imaging splenorenal

shunts [40]. In these cases, color Doppler US may be useful to locate and evaluate patency of the shunts through minimal bowel gas and backscatter [40]. But it may be difficult to elicit color signal from within the synthetic graft or detect the flow within the mesoatrial and splenorenal shunts, which are located deep in the abdomen [40]. Signs of patency include visualization of flow through the communication between the systemic and portal veins, absence of post-stenotic jet and visualization of appropriately directed flow in the shunted splanchnic vein toward the shunt and systemic vein [40]. Detection of color-coded flow within the shunt itself (Fig. 10a), the splanchnic vein and systemic vein (Fig. 10b) adjacent to the shunt is a strong indication of shunt patency [40–42], keeping in mind that shunt dysfunction due to stenotic non-occlusive disease may still be present. In cases where the site of the anastomosis or the shunt cannot be visualized directly by US, reversal of flow after surgery (i.e., hepatofugal flow) in the intrahepatic portal veins can be used as a reliable indirect sign of shunt patency [42,49]. However, it should be kept in mind that this finding is not useful in patients with a reduced-diameter or selective shunts [18,50]. On the other hand, detection of new or increase in the size of previously present portosystemic collateral vessels on follow-up imaging can be used as an indirect sign to suggest shunt thrombosis or




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Fig. 11. Thrombosed C-type mesocaval graft in a 72 year-old female with portal hypertension due to idiopathic liver cirrhosis. [a and b] Axial T2-weighted MRI of the abdomen in two consecutive cuts showing high signal intensity within the mesocaval graft indicating thrombosis. [c] Axial contrast-enhanced CT of the abdomen in the venous phase showing absence of contrast opacification of the thrombosed C-type mesocaval graft. [d] Volume rendered reconstruction showing the C-type mesocaval graft, significant collateral circulation and splenomegaly. [Mesocaval graft = double arrow, superior mesenteric vein branch = open arrow, IVC = asterisk, spleen = sp].

dysfunction [40]. While imaging grafts, real-time scanning, can identify the echogenic walls of the synthetic graft, then either color or spectral Doppler sonography could be used to establish patency [40]. Measuring flow velocities has been well established in the medical literature to suggest non-occlusive malfunction of TIPS (ie, stenosis). As the presence of color-coded flow in the SPSS may not be sufficient to exclude shunt dysfunction when the patient presents with new signs of increased portal pressure, flow measurement can be helpful to diagnose stenotic non-occlusive disease resulting in shunt dysfunction. Suggested signs of stenosis of SPSS include an abnormally high (>190 cm/s) or abnormally low (50 cm/s) compared with the prior examination [51]. As previously discussed, imaging of splenorenal anastomosis might be challenging and knowledge of the optimal scanning planes is essential. Scanning from a left subcostal approach, the splenic limb of the shunt can be visualized dorsally for a considerable distance. On the other hand, the left renal vein flow, which is normally directed perpendicular to the splenic vein, can be best detected by scanning through the left flank [40].

5.2. Magnetic resonance imaging MRI is an accurate and reliable non-invasive method for evaluation of liver parenchyma, portal and systemic circulation and SPSSs [52]. It encompasses many of the advantages of CT, US, and conventional angiography. MRI enables imaging of the liver in multiple planes and delineates the vascular structures by means of the “flow void” phenomenon in great detail without the use of intravenous contrast material [52]. Rapidly flowing blood in the vessels produces no detectable signal indicating shunt patency (Fig. 4a), in contrast to absent, slow or turbulent flow which produce a highintensity signal (Fig. 11a and b). The ability to obtain multiplanar images allows visualization of SPSSs of different orientations. MRA, using time-of-flight or dynamic multiphase, gadolinium enhanced imaging (Fig. 4b), is another method to evaluate shunt patency [53]. MR imaging protocol for the assessment of SPSSs typically includes anatomical assessment of the abdominal organs with pre-contrast axial, coronal and sagittal T1-weighted images, in addition to axial and coronal T2-weighted images. In patients with good renal function, dynamic multiphase gadolinium-enhanced MRA of the abdomen is performed during the arterial and portal venous phases of vascular enhancement. In patients with reduced renal function, time-of-flight MRA, which is a flow-based imaging




Fig. 12. 36 year-old female patient with Budd–Chiari syndrome, presented for evaluation of the portosystemic shunt. [a] Arterial portography performed by superior mesenteric artery injection to evaluate the shunt and localize the anastomosis. Both the main portal vein and IVC show good opacification indicating shunt patency. [b] Direct shuntography, after localizing the anastomosis, showing the patent side-to-side portocaval shunt with contrast flowing into the IVC as an outflow tract. [IVC = asterisk, portal vein = arrow, anastomosis = double arrow].

method, can be performed to assess vascular structures and the shunt. MRI is expensive and time consuming, and can be suboptimal and challenging in critical patients. The need for sedation in children adds additional cost and risk. In addition, visualization of the vascular structures and SPSSs can be limited in patients who have had prior embolization with steel coils in the area of interest [43]. Another pitfall in MRI is that the vascular anatomy must be integrated over several consecutive cuts (Fig. 11a and b). 5.3. Computed tomography Multiphasic contrast-enhanced CT is a relatively non-invasive and effective modality in the evaluation of liver morphology, portal and systemic venous vasculature, and SPSS [45]. Imaging processing techniques such as multiplanar reconstruction (MPR) (Figs. 5b and c, 6b and 8a), volume-rendered reconstruction (VR) (Figs. 5d, 7b, 8b and 11d), and maximum intensity projection (MIP) (Figs. 4c and 7a) have added much value in the illustration of the course and patency of the SPSSs by providing a global 3dimentional view of different vascular structures and variations of shunt anatomy. In addition, CT is useful in the assessment of the enhancement pattern of the liver parenchyma and can illustrate signs of portal hypertension, such as splenomegaly and collateral circulation (Figs. 8b and 11d), as well as other pathologies. CT has higher spatial resolution than ultrasound and MRI. It is less operator dependent than ultrasound and less expensive and sensitive to motion when compared to MRI. However, CT imaging involves radiation exposure and injection of contrast material which may exacerbate pre-existing renal impairment. 5.4. Conventional angiography and venography Angiography has been the definitive method of evaluating portal circulation and portosystemic shunts for some time. It is an invasive, expensive imaging modality and the anatomically isolated portal system may be difficult to opacify [54]. Over the last few decades, due to recent technical advances, evaluation of the portal vasculature and SPSSs using minimally invasive procedures became possible, by splenoportography, arterial portography and catheterization of the shunt through a systemic venous or a transhepatic portal venous access.

Splenoportography, now seldom used, is performed by direct puncture of the spleen using a 21-gauge needle and injection of contrast after confirming the intra-splenic needle position. Although splenoportography can demonstrate some types of SPSSs, it is of no use in the evaluation of shunts in which the spleen has been removed or in cases of severe portal hypertension with reversal of flow in the splenic vein [55]. In addition, the risk of iatrogenic splenic aneurysm, bleeding and emergency splenectomy following splenoportography must be considered. Indirect arterial portography performed by superior mesenteric, splenic or celiac angiography and acquisition of delayed images during portal venous phase, is used to evaluate portal perfusion, detect the presence of spontaneous portosystemic collaterals and localize the site of anastomosis (Figs. 12a and 13a and e). Evaluation of the SPSS may be possible using this technique, particularly when CT-like images are obtained on modern flat-panel detector Carm angiography using rotational 3-dementional acquisition [56]. The portal vein may fail to opacify if its flow is hepatofugal because splanchnic venous return does not enter the portal vein and due to preferential opacification of collaterals caused by rapid shunting of blood away from the native circulation [45,49]. Portal vein thrombosis can be mistakenly diagnosed using this technique if these pitfalls are not recognized. Percutaneous transhepatic portography will generally demonstrate only the intrahepatic portal system unless there is severe cirrhosis with reversal of blood flow. However, with advanced catheter technique, direct catheterization of the shunt is possible to directly evaluate patency. However, catheterization of the shunt is frequently performed through systemic venous access (Figs. 12–15), which has higher rate of success and lower risk of bleeding when compared to transhepatic access. Shunt catheterization enables direct pressure measurement in the shunt, as well as in the portal and systemic venous ends of the shunt. Pressure measurement in the shunt enables reliable detection of hemodynamically significant stenosis, which cannot be performed using any of the previously discussed imaging modalities. In addition, successful long-term outcome of SPSSs is usually predicted by a pressure gradient between the portal vein and the IVC of more than 10 mmHg. This pressure gradient is required for adequate blood flow across the shunt, even in the presence IVC compression by the caudate lobe of the liver [57]. Therefore, it has been suggested that maintaining a portocaval pressure gradient between 10 and 13 cm




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Fig. 13. [a] Indirect arterial portography performed by superior mesenteric artery injection showing good opacification of the superior mesenteric and portal veins with no contrast seen in the IVC or the shunt. [b] Subsequent cavogram showing good opacification of the IVC and minimal contrast reflux within the portocaval shunt [curved arrow] at the level of the surgical clips. [c] Direct shuntography after catheterizing the portocaval graft from a jugular venous access showing absence of opacification of the shunt or IVC with good visualization of the superior mesenteric and portal veins. [d] Direct shuntography after balloon angioplasty of the shunt showing partial opacification of a kinked graft. [e] Indirect arterial portography after stenting the portocaval graft, showing good opacification of the stented graft. [IVC = asterisk, portal vein = arrow, superior mesenteric vein = open arrow, portocaval graft = double arrow, kink = arrowhead].

H2 O (13.6–17.6 mmHg) is optimal for portal decompression [34]. Because shunt dysfunction can be asymptomatic, it has been recommended to evaluate any kind of SPSS at an annual interval with a percutaneous shuntogram or a hepatic vein pressure measurement [34]. Cavogram can be performed at the same time to evaluate IVC compression by the enlarged caudate lobe, as a cause of shunt dysfunction, specifically in patients with Budd–Chiari syndrome. Angiography involves a certain risk to patients who are debilitated by chronic liver disease, which is often associated with renal and cardiac impairment that may be exacerbated by iodinated contrast agents. Obtaining multiple views increases the radiation exposure and contrast dose [45]. However, with the flat-panel detector C-arm angiography and multiphasic CT 3-dimentional reconstruction techniques, images can be assessed in any plane

after acquisition, thus reducing contrast dose and radiation exposure. As a consequence, in the presence of alternative imaging modalities, direct angiography is used only when there is significant clinical doubt of shunt patency or when interventional management of a dysfunctional shunt is required. 6. Role of interventional radiology Interventional radiologists play a pivotal role in the assessment of SPSSs, detection and management of complications, and followup. Stenosis of a SPSS may progress to occlusion and potentially serious consequences such as recurrent life-threatening variceal bleeding. Detection and timely management of SPSS stenosis or occlusion improves survival and decreases the risk of progressive




Fig. 14. Thrombosed mesocaval graft in a 23 year-old female with Budd–Chiari syndrome. [a] Digital subtraction direct shuntography using a 4 Fr. catheter introduced from the right femoral vein through the graft, with its tip in a jejunal branch of the superior mesenteric vein. It shows no opacification of the thrombosed mesocaval shunt or IVC. [b] Balloon dilatation after mechanical thrombectomy and [c] direct shuntography post-dilatation showing opacification of the graft [double arrow] and contrast flow in the IVC. [IVC = asterisk, superior mesenteric vein/branches = open arrow].

liver failure or recurrent bleeding. Several interventional techniques have been reported in the management of SPSS stenosis or occlusion including angioplasty with or without stent placement [34,58], percutaneous mechanical thrombectomy [33] and local thrombolytic infusion [58]. In cases of SPSS stenosis, balloon dilatation may improve flow and relieve symptoms [59]. When there is total occlusion of the shunt, recanalization and angioplasty can partially or completely restore blood flow within the shunt (Figs. 13d, 14c and 15e). Primary patency rates after angioplasty for SPSS stenosis have been poor in patients with Budd–Chiari syndrome and multiple dilatation may be required to maintain patency of stenosed SPSSs. Re-thrombosis of the shunt might be related to a preexisting prothrombotic disorder, the turbulent flow in shunts and the presence of IVC compression by the caudate lobe. Angioplasty with stent insertion can be performed if there is immediate recoil or inadequate response to balloon dilatation or can be performed after recurrent stenosis or occlusion [60]. Mechanical thrombectomy and thrombolysis can be successful, especially in patients with early shunt thrombosis. Thrombectomy can be performed, after catheterization of the thrombosed graft, by passing an adequatelysized inflatable balloon through the graft multiple times. It can be repeated till significant clearance of thrombus load is achieved and

blood flow is resumed within the shunt, followed by balloon dilatation (Fig. 14). Baijal et al. reported a successful thrombectomy using a 7-Fr Swan-Ganz catheter followed by balloon dilatation across the shunt [33]. Complications such as embolization from the graft, venous perforation, retroperitoneal hemorrhage and graft infection are rare. Several techniques are available for catheterization of the portal venous system, which can provide access to the SPSS. The percutaneous transhepatic approach has been widely adopted by many radiologists. However, passage through a thrombosed segment of the portal vein may be difficult. It can also be difficult in patients with a large amount of ascites or hematoma around the liver. It has been noted that successful catheterization of occluded interposition grafts from the cava to mesenteric vein can be achieved in a high percentage of cases [34], after localizing the ostium through a transmitted sensation of grittiness in the area of anastomosis or visualization of mild contrast reflux into the shunt (Fig. 13b) [33]. To facilitate angiographic localization of the thrombosed graft, especially in patients with delayed diagnosis, Cope suggested placing a radiopaque marker at the graft ostium during surgical creation of the shunt [34]. When the graft or its anastomotic side is totally occluded, then gentle probing is performed




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Fig. 15. 23 year-old female with known Budd–Chiari syndrome, status post IVC and portosystemic graft stenting, presented one year later with signs of portal hypertension. [a] Digital subtraction cavogram and [b] direct shuntography showing a narrowed IVC [arrowhead] at the distal aspect of the caval stent [right-angled arrow], significant systemic venous collaterals and a thrombosed portosystemic stent [double arrow]. [c] Cavogram after deploying a second IVC stent [right-angled arrow] shows resolution of the IVC stenosis. [d] Balloon dilatation of the thrombosed portocaval shunt and [e] direct shuntography after deploying a second stent showing good opacification of the stented graft [double arrow] and IVC [right-angled arrow].

by advancing the catheter over the guide-wire or by using various types of flexible hydrophilic guide-wires until a sudden advance of the catheter indicates passage into the graft. Forceful use of stiff catheters or guide-wires may cause perforation and subsequent retroperitoneal bleed. In patients with acute variceal hemorrhage due to occluded SPSS, bleeding can be controlled after successful catheterization of the shunt, by occluding the bleeding varices with gelfoam or coils and balloon angioplasty of the shunt to decrease the portal pressure gradient. Percutaneous dilatation of SPSSs is a life-saving procedure, and is therefore recommended in all patients with suspected graft occlusion and on all recently closed direct portocaval or splenorenal shunts with acute variceal hemorrhage. IVC angioplasty/stenting has been combined with SPSS creation if the IVC is severely compressed by an enlarged caudate lobe for the shunt to function properly [28]. Using the same principle, combined IVC stenting with catheterization and angioplasty of the thrombosed SPSS has been performed for management of shunt dysfunction (Fig. 15). Venographic approaches may be from the femoral or transjugular route or rarely direct percutaneous

transhepatic puncture into the hepatic veins. Dilatation alone with an adequately-sized balloon opens up the IVC in most cases in patients with IVC stenosis. Stents have been used in the IVC when balloon dilatation alone was insufficient because of recoil or recurrent stenosis, especially with extrinsic compression by an enlarged caudate lobe. Stent placement ensures adequate patency of the IVC and decreases the likelihood of subsequent recurrent SPSS thrombosis due to decreased flow through the outflow tract (i.e., IVC). Finally, when the occluded SPSS cannot be recanalized, a TIPS procedure can relieve the recurrent symptoms.

7. Conclusion SPSS formed the mainstay of the management of portal hypertension and used to relieve portal hypertension by converting the portal vein to an outflow systemic venous circulation. Although it is still performed in selected cases, its use has been challenged by the emergence of new interventional techniques and liver transplantation.




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The main limitations of shunt surgery currently are declining expertise and perioperative mortality of 10–20%. Knowledge of surgical types and flow dynamics after SPSS creation is pivotal in interpretation of imaging studies. Management requires a multidisciplinary team approach with hepatology, hematology, surgical, and radiology expertise. Funding information None. Conflict of interest statement No conflict of interest. References [1] Shneider BL. Portal hypertension. In: Suchy FJ, Sokol RJ, Balistreri WF, editors. Liver disease in children. New York, NY: Cambridge University Press; 2007. p. 138–62. [2] Dib N, Oberti F, Calès P. Current management of the complications of portal hypertension: variceal bleeding and ascites. CMAJ 2006;174(10):1433–43. [3] Wolff M, Hirner A. Current state of portosystemic shunt surgery. Langenbecks Arch Surg 2003;388(3):141–9. [4] Lillegard JB, Hanna AM, McKenzie TJ, Moir CR, Ishitani MB, Nagorney DM. A single-institution review of portosystemic shunts in children: an ongoing discussion. HPB Surg 2010;2010:964597. [5] Orug T, Soonawalla ZF, Tekin K, Olliff SP, Buckels JA, Mayer AD. Role of surgical portosystemic shunts in the era of interventional radiology and liver transplantation. Br J Surg 2004;91(6):769–73. [6] Emre S, Dugan C, Frankenberg T, Hudgins LC, Gagliardi R, Artis AT, et al. Surgical portosystemic shunts and the Rex bypass in children: a single-centre experience. HPB [Oxford] 2009;11(May (3)):252–7. [7] Copelan A, Remer EM, Sands M, Nghiem H, Kapoor B, Diagnosis. Management of Budd Chiari syndrome: an update. Cardiovasc Intervent Radiol 2015;38(Feb (1)):1–12. [8] Brems JJ, Hiatt JR, Klein AS, Millis JM, Colonna JO, Quinones-Baldrich WJ, et al. Effect of a prior portasystemic shunt on subsequent liver transplantation. Ann Surg 1989;209(1):51–66. [9] Horton JD, San Miguel FL, Membreno F, Wright F, Paima J, Foster P, et al. Budd–Chiari syndrome: illustrated review of current management. Liver Int 2008;28(4):455–66. [10] Garcia Jr N, Sanyal AJ. Portal hypertension. Clin Liver Dis 2001;5(May (2)):509–40. [11] Jarnagin WR. Blumgart’s surgery of the liver, biliary tract and pancreas. Philadelphia, PA: Elsevier Saunders; 2012. [12] Chattopadhyay S, Nundy S. Portal biliopathy. World J Gastroenterol 2012;18(Nov (43)):6177–82. [13] Lopez-Santamaria M, Migliazza L, Gamez M, Murcia J, Diaz-Gonzalez M, Camarena C, et al. Liver transplantation in patients with homozygotic familial hypercholesterolemia previously treated by end-to-side portocaval shunt and ileal bypass. J Pediatr Surg 2000;35(4):630–3. [14] Warren WD, Zeppa R, Fomon JJ. Selective trans-splenic decompression of gastroesophageal varices by distal splenorenal shunt. Ann Surg 1967;166(Sep (3)):437–55. [15] de Ville de Goyet J, D’Ambrosio G, Grimaldi C. Surgical management of portal hypertension in children. Semin Pediatr Surg 2012;21(Aug (3)):219–32. [16] Orloff MJ, Isenberg JI, Wheeler HO, Daily PO, Girard B. Budd–Chiari syndrome revisited: 38 years’ experience with surgical portal decompression. J Gastrointest Surg 2012;16(2):286–300 (discussion 300). [17] Sigalet DL, Mayer S, Blanchard H. Portal venous decompression with H-type mesocaval shunt using autologous vein graft: a North American experience. J Pediatr Surg 2001;36(1):91–6. [18] Rikkers LF, Sorrell WT, Jin G. Which portosystemic shunt is best? Gastroenterol Clin North Am 1992;21(1):179–96. [19] Rosemurgy AS, McAllister EW, Goode SE. Direction or reversal of preshunt portal blood flow as determinants of outcome up to 1 year after small-diameter prosthetic H-graft portacaval shunt. J Surg Res 1995;58(Apr (4)):432–4. [20] Shields R. Small-diameter PTFE portosystemic shunts: portocaval vs mesocaval. HPB Surg 1998;10(6):413–4. [21] Drapanas T. Interposition mesocaval shunt for treatment of portal hypertension. Ann Surg 1972;176(Oct (4)):435–48. [22] Slakey DP, Klein AS, Venbrux AC, Cameron JL. Budd–Chiari syndrome: current management options. Ann Surg 2001;233(Apr (4)):522–7. [23] Fisher NC, McCafferty I, Dolapci M, Wali M, Buckels JA, Olliff SP, et al. Managing Budd–Chiari syndrome: a retrospective review of percutaneous hepatic vein angioplasty and surgical shunting. Gut 1999;44(4):568–74. [24] Cameron JL, Maddrey WC. Mesoatrial shunt: a new treatment for the Budd–Chiari syndrome. Ann Surg 1978;187(4):402–6. [25] Mirkovic D, Stankovic N, Jevtic M, Mitrovic M, Jovanovic M. Mesoatrial shunt in Budd–Chiari syndrome. Vojnosanit Pregl 2009;66(1):69–73.

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Markers of hepatic regeneration associated with surgical attenuation of congenital portosystemic shunts in dogs.

Bleeding esophageal varices: today's role of portosystemic shunts.

Percutaneous Portosystemic Shunts: TIPS and Beyond.

Color Doppler imaging of portosystemic shunts.

Passive expansion of sub-maximally dilated transjugular intrahepatic portosystemic shunts and assessment of clinical outcomes.

Prenatal sonographic diagnosis of intrahepatic portosystemic shunts.

Status epilepticus after ligation of portosystemic shunts.

Current concepts in congenital portosystemic shunts.

Morphology of splenocaval congenital portosystemic shunts in dogs and cats.

Surgical attenuation of spontaneous congenital portosystemic shunts in dogs resolves hepatic encephalopathy but not hypermanganesemia.

Technical advances in transjugular intrahepatic portosystemic shunts.

Diagnostic radiologists and nuclear medicine.

Role of parallel transjugular intrahepatic portosystemic shunts in patients with persistent portal hypertension.

Transhepatic Embolization of Congenital Intrahepatic Portosystemic Venous Shunts with Associated Aneurysms.

Outcomes of transjugular intrahepatic portosystemic shunts for ascites.

The peritoneal complications of ventriculo-peritoneal shunts.

Mechanical complications in shunts.

The inheritance of extra-hepatic portosystemic shunts and elevated bile acid concentrations in Maltese dogs.

Spontaneous portosystemic shunts in noncirrhotic patients presenting with encephalopathy.

Transjugular intrahepatic portosystemic shunts in liver transplant recipients.

Abdominal and genitourinary complications following ventriculoperitoneal shunts.

Transjugular intrahepatic portosystemic shunts: preliminary results in 25 patients.

Percutaneous intervention in portosystemic shunts in Budd-Chiari syndrome.

Color Doppler sonography in spontaneous splenorenal portosystemic shunts.