Interventional Radiology in the Multidisciplinary Management of Liver Lesions: Pre- and Postoperative Roles

• Preoperative Roles
• Locoregional Therapies
• Bridging Patients with HCC to Liver Transplantation
• Recommendation
• Downstaging Patients with HCC for Liver Transplantation
• Recommendations
• Hepatic Optimization Prior to Resection
• Portal Vein Embolization
• Recommendations
• Preoperative Biliary Drainage
• Recommendations
• Transjugular Intrahepatic Portosystemic Shunt
• Direct Intrahepatic Portocaval Shunt
• Recommendations
• Balloon-Occluded Retrograde Transvenous Obliteration of Gastric Varices
• Recommendations
• Postoperative Roles
• Management of Postoperative Biliary Complications
• Percutaneous Dilatation of Biliary Strictures
• Recommendations
• Percutaneous Biliary Diversion for Postoperative Biliary Leak
• Recommendations
• Management of Posttransplant Arterial Complications
• Hepatic Artery Stenosis
• Hepatic Artery Thrombolysis
• Recommendation
• Management of Posttransplant Venous Complications
• Conclusion
• References

Abstract

The management algorithm for patents with liver lesions, most often hepatocellular carcinoma (HCC) or colorectal cancer metastasis, are complex, ever-changing, and involve multiple treatment modalities including chemotherapy, external-beam radiation, surgery, and locoregional therapies (LRTs). This complexity necessitates a multidisciplinary approach including hepatologists, oncologists, hepatobiliary surgeons, radiation oncologists, and interventional radiologists to coordinate and deliver the complex care that these patients need in a timely manner. The interventional radiologist and hepatobiliary surgeon work closely together in both the pre- and postoperative setting. Preoperative roles include delivering LRTs to patients with HCC and interventions aimed at hepatic optimization prior to resection or transplantation. LRT in this setting is performed either to bridge the patient to transplant or to downstage the initially nontransplant candidate so appropriate transplant criteria are met. Postoperative roles include the management of biliary and vascular complications that may occur after resection or transplantation.

Preoperative Roles

Locoregional Therapies

The role of the interventional radiologist in the preoperative management of liver tumors usually falls into one of two categories: to perform locoregional therapies (LRTs) for hepatocellular carcinoma (HCC) or for hepatic optimization prior to surgery.

Locoregional therapies are performed for disease control prior to definitive treatment or disease downstaging so a patient is a suitable candidate for definitive treatment. To achieve these ends, a variety of LRTs are available. Transarterial options include bland transarterial embolization (TAE), transarterial chemoembolization (TACE) with a variety of chemotherapeutic drugs, and transarterial radioembolization (TARE) with yttrium-90 (Y-90). Percutaneous ablative technologies include radiofrequency ablation (RFA), microwave ablation, cryoablation, and irreversible electroporation (IRE).

Bridging Patients with HCC to Liver Transplantation

Liver transplantation is the standard of care for patients with HCC that meets the Milan Criteria.[1] For these patients, the 5-year survival is at least 70% and equals the 5-year survival seen in patients undergoing liver transplant for nontumor indications.[1] The scarcity of liver donors, however, can lead to disease progression and subsequent waitlist dropout. Dropout rates of up to 32% at one year have been reported.[2] As such, a variety of LRTs have been used in an attempt to control disease and maintain patients on the liver transplant waitlist.

The choice of LRTs used is highly variable; dependent on the treating institution as well as HCC size, number, and location. For tumors less than 3 cm, percutaneous RFA has demonstrated excellent disease control. In a large review of 216 patients with HCC < 2 cm, a sustained complete response in 97% of lesions was observed.[3] Microwave ablation may be used to treat lesions of this size close to the portal or hepatic veins. Due to a different method of heating, microwave ablation is felt to be less susceptible to the “heat-sink” effect that can lead to incomplete treatment.[4] Cryoablation, the process of using extreme cold to destroy tissues, has not been widely used in the liver. One concern has been tumor lysis syndrome, also termed “cryoshock.” Although rare, this has been ascribed to tissue necrosis that is directly exposed to the blood stream resulting in thrombocytopenia, and renal and hepatic failure.[5] Newer technical advances including smaller probe size and the use of Argon gas-based systems has renewed interest and research in cryoablative therapies. Irreversible electroporation is a new technology that uses electrical pulses to create irreversible pores in cell membranes that cause apoptosis.[6] These pulses do not affect the extracellular matrix, leaving blood vessels and bile ducts uninjured. In a small early report of IRE in 44 patients with different tumors, 14 HCCs, a recurrence-free survival of 98% was observed for lesions < 3 cm. Note is made of no response for HCC > 5 cm in this series.[7] Combination therapy with TACE prior to RFA may also be performed, with one such case detailed in [Fig. 1].

A transarterial approach is often preferred in the setting of multiple tumors or tumors > 3 cm. Which embolic agent is used continues to be a matter of debate. Controversy over the superiority of TACE to TAE persists, although a large meta-analysis did reveal a survival benefit in patients treated with TACE with no benefit observed in those treated with TAE.[8] [9] Drug-eluting beads loaded with doxorubicin have recently been introduced into clinical practice (DC/LC beads, Biocompatible, London, UK). An early report of their use found improved tolerability and decreased liver toxicity with drug-eluting beads compared with conventional TACE, although treatment superiority to TACE was not demonstrated.[10] Transarterial radioembolization with Y-90 has received approval from the Food & Drug Administration for unresectable HCC and as a bridge to transplantation. Response rates of 39 to 47% have been reported with a time to progression of 10 months.[11] [12] [13]

There is growing evidence that the use of these LRTs for patients with > 1 HCC or an HCC > 3 cm decreases waitlist dropout when a wait time of  > 3 months is expected.[14] [15] [16] [17] These results have led to the widespread use of LRTs for patients on the transplant list, with up to 65% of waitlisted patients receiving some form of LRT depending on the region.[18] Patients with a single HCC < 3 cm who are closely monitored do not need LRT because of low rates of waitlist dropout.

Recommendation

Evidence supports the use of LRTs for patients with HCC who meet the Milan Criteria awaiting transplantation for the purpose of decreasing the risk of waitlist dropout. The choice of LRT depends on the size, number, and location of the HCC(s) to be treated.

Downstaging Patients with HCC for Liver Transplantation

A recent working-group statement defined downstaging as the use of LRT for HCC with the goal of meeting “acceptable” criteria for liver transplantation.[15] Experience with liver transplantation in patients who did not initially meet the Milan Criteria, but had sufficient response to LRT to subsequently qualify continues to grow.[11] [19] [20] A treatment response in these patients selects those with favorable tumor biology who will respond well to liver transplant. Heterogeneity in the size and number of tumors treated, combined with differences in response criteria, and endpoints, makes evaluating the literature difficult.

Locoregional therapies used for patients not initially a candidate for liver transplant includes the modalities described above. The size, number, and location of the lesions that require treatment will determine the modality by the previously described considerations. Response to treatment is determined by residual enhancement on dynamic, triple-phase contrast enhanced computed tomography (CT) or magnetic resonance imaging (MRI) obtained 4 to 6 weeks after treatment. Successful downstaging often requires repeat intervention, or a combination of interventions to be performed.

Perhaps the greatest experience with HCC downstaging by LRT is from University of California-San Francisco (UCSF), where TACE was the primary LRT used. In their experience with 61 patients who did not meet conventional criteria for liver transplantation, downstaging was successful in 42 patients (70.5%).[20] Of these patients, 37 went onto liver transplant with six awaiting transplant at the time of publication. None of the patients had recurrence of HCC at follow-up with 1- and 4- year survival rates of 96% and 92%, respectively. The theory of downstaging as a method to select patients with favorable tumor biology was supported, as none of the explanted livers were found to have poorly differentiated HCCs.

Transarterial radioembolization has also been used to downstage patients with HCC prior to liver transplantation. At Northwestern University, the efficacy of TARE at downstaging United Network for Organ Sharing (UNOS) T3 to T2 disease was compared with TACE in 86 patients with HCC. In this study, successful tumor downstaging (58% vs. 31%) and overall survival (35.7 months vs. 18.7 months) was significantly higher in patients treated with TARE compared with TACE. In this study, nine TARE patients and 11 TACE patients went onto liver transplantation, with the 1-year recurrence-free survival after transplantation not significantly different.[21]

Although UCSF supports a downstaging strategy in patients with four or five small HCCs as long as the total tumor diameter is ≤ 8 cm, only four such patients went onto transplant. As such, downstaging in patients with more than three HCCs has not been universally accepted. Different criteria recommended downstaging for patients with a single HCC ≤ 8 cm or two to three HCCs as long as each HCC is ≤ 5 cm and total diameter is ≤ 8 cm. Other additional recommendations include a 3-month observation period after Milan Criteria are met before priority transplant listing, an alpha-fetoprotein (AFP) level < 500 ng/mL in those who initially had an AFP >1000 ng/mL, and routine CT scans of the chest and multiphase CT/MRIs of the abdomen.[15]

Recommendations

Downstaging HCC in patients who do not initially meet Milan Criteria identifies a group of patients suitable for curative treatment with liver transplant. The choice of LRT depends on the size, number, and location of the HCC(s) to be treated.

Hepatic Optimization Prior to Resection

Portal Vein Embolization

Transplantation for HCC and complete resection for cholangiocarcinoma or colorectal cancer metastasis offer the best chance for long-term survival. As surgical techniques have been refined, the operative mortality rates at high-volume centers have dropped to less than 5%. Amount of blood loss and the number of hepatic segments resected remain independent predictors of morbidity and mortality.[22] Advanced disease at presentation has previously limited the number of patients who were considered surgical candidates due to the large amount of liver that would need to be resected to clear the patient of disease.

Over the past decade, however, the emphasis has shifted from the maximum amount of liver that can safely be resected to the minimum future liver remnant (FLR) that is needed to maintain hepatic function postoperatively.[23] [24] Identifying patients with an anticipated FLR that would result in marginal liver function, predisposing to cholestasis, fluid retention and other complications, or inadequate liver function, leading to transplantation or death, is critical. These patients are candidates for preoperative portal vein embolization (PVE) to induce hypertrophy of the nonembolized segments and augment hepatic reserve.

The minimum safe volume of the FLR varies from patient to patient, depending on background liver disease and body size. As a result, the percentage of the anticipated FLR volume to the total liver volume (TLV), as calculated from the patient's body surface area, is most relevant.[25] For patients with a noncirrhotic liver, the minimum FLR has been reported to be 25%.[26] More recently, this number has been lowered to 20% after a review of 301 consecutive patients who underwent extended right hepatectomy identified no difference in liver insufficiency or death in patients with a FLR between 20.1% and 30% compared with those with an FLR > 30%.[27] Due to the diminished regenerative capacity of cirrhotic livers and livers treated with high-dose chemotherapy or have steatohepatitis, a higher FLR is required. A FLR of > 30% for injured liver and > 40% in cirrhotic patients is used at several institutions, although strong evidence supporting this cutoff is lacking.[25] [28] [29] [30]

Portal vein embolization is typically performed 4 to 6 weeks prior to hepatic resection to allow time for FLR hypertrophy. Portal vein embolization may be performed percutaneously by accessing either the ipsilateral (i.e., side to be resected) or contralateral (i.e., side to be remain after surgery) portal vein or intraoperatively via the transileocolic venous approach. The approach chosen is based on several factors, including the extent of embolization and surgery to be performed, embolic agent to be used, and operator preference and experience.[31] The case of an ipsilateral PVE performed with glue and Ethiodol is provided in [Fig. 2].

The ipsilateral percutaneous approach has the distinct advantage of not instrumenting the FLR and allows for easy catheterization of segment 4 branches.[32] Awareness of patient disease is critical so puncture through tumor can be avoided if possible, to minimize the theoretical risks of bleeding or seeding. The contralateral percutaneous approach offers technically easier catheterization of the right portal branches and embolization in the direction of flow. The major drawback of this approach is access is made through the FLR. If complications were to occur, they could make the planned surgical resection difficult or impossible.

More recently, some have advocated TACE prior to PVE in patients with HCC awaiting hepatic resection. The rationale for this approach is to increase FLR hypertrophy and prevent compensatory arterialization of the diseased liver after PVE, which could theoretically induce rapid disease progression and to embolize any arterioportal shunts within the tumor or diseased liver that can limit the hypertrophy. Two retrospective studies that examined this approach demonstrated an increased rate of hypertrophy and longer recurrence-free survival in patients treated with TACE and PVE compared with those treated with PVE only.[33] [34] The primary drawbacks of this approach are the need for a second procedure and an additional waiting period needed between TACE and PVE to prevent the risk of hepatic infarction.

The ability of preoperative PVE embolization to increase hepatic function of the hypertrophied FLR has been proven biochemically as well as volumetrically in both cirrhotic and noncirrhotic livers.[35] [36] [37] This hypertrophy been shown to be associated with decreased complications, shorter hospital stays, increased resectability, and increased disease-free survival in patients with cirrhosis and HCC.[38] [39] Portal vein embolization as part of a one- or two-staged approach has also been shown to increase the resectability of colorectal cancer liver metastasis by increasing a previously inadequate FLR.[40] [41] [42]

However, 2 to 20% of patients with cirrhosis can be expected to have no significant increase in FLR after a technically successful PVE. Theories behind the lack of response observed in some patients include recanalization of the portal vein and arterioportal shunting.[31] [43] It has been proposed that this absence of hepatic hypertrophy can be used as an indicator of hepatic inability to regenerate and a contraindication to major hepatic resection.[38] Similarly, in a review of 112 patients who underwent preoperative PVE prior to extended right hepatectomy a post-PVE FLR of < 20% and a < 5% FLR hypertrophy had higher overall, major and liver-related complications, and a higher 90-day mortality rate.[44] Recently, the kinetic growth rate at which FLR hypertrophy occurs has been demonstrated to be an even better predictor of postoperative morbidity and mortality than conventional static volumetric parameters.[45]

Complications related to PVE are rare, but include hematoma, arterial pseudoaneurysm, abscess, propagation of portal vein thrombosis, and portal hypertension. A large meta-analysis, which included both percutaneous and intraoperative approaches, listed morbidity and mortality after PVE at 2.2% and 0% respectively.[37]

Recommendations

Portal vein embolization is a safe and effective procedure for increasing hepatic reserve in patients with inadequate anticipated FLR, < 20% without cirrhosis, < 30% in injured liver such as high-dose chemotherapy and steatohepatitis and < 40% with cirrhosis. Lack of response to PVE has been associated with worse postoperative outcomes.

Preoperative Biliary Drainage

Significant improvements in perioperative and long-term outcomes have recently been observed following surgical resection of cholangiocarcinoma. Current retrospective series list morbidity and mortality rates between 14 to 67% and 0 to 20%, respectively.[46] [47] [48] [49] Although there is little debate about the role of percutaneous biliary drainage in the setting of cholangitis prior to surgery, the role of routine preoperative biliary drainage (PBD) for malignant biliary obstruction remains a point of much debate.[50] [51] [52] This debate is only further complicated by the heterogeneity of malignant obstructions and relative rarity of cholangiocarcinoma.

A large meta-analysis of randomized control studies that examined PBD for malignant obstruction demonstrated no improvement in overall death with increased complication rates and longer hospital stays.[53] In this analysis, less than 25% of patients had cholangiocarcinoma and less than 20% of patients had hepatic resection. Similarly, two Cochrane reviews of PBD for malignant biliary obstruction demonstrated no survival benefit with increased serious morbidity.[54] [55] The ultimate conclusion of both reviews was that sufficient evidence was not available to support or refute routine PBD. Due to the increased risk of adverse complications, routine drainage was not recommended outside of randomized controlled trials. Again, the majority of patients in these reviews were patients with low obstructions.

A smaller review of patients with cholangiocarcinoma treated with resection with or without PBD observed an increased incidence of infectious complications without improved morbidity or mortality.[56] More recently, a role for routine PBD of the FLR prior to major right hepatectomy for cholangiocarcinoma has been advocated by some investigators.

Biliary drainage may be performed percutaneously or endoscopically, with endoscopic drainage often preferred because of the less-invasive nature of the procedure. If endoscopic drainage fails, percutaneous drainage can be performed with relatively low morbidity. A variety of plastic and covered or uncovered self-expanding metal stents are available for the gastroenterologist and interventional radiologist. A multidisciplinary approach is critical to select the type and site of stent to be deployed with the best approach, tailored according to the planned hepatic resection.

The recently released Multicenter European study examined 366 patients who underwent left or extended right hepatectomy for hilar cholangiocarcinoma.[57] One hundred eighty of these patients had preoperative biliary drainage, either percutaneous or endoscopic, and 186 did not. Overall postoperative mortality, overall morbidity, and severe morbidity were not significantly different between the two groups. A further analysis of patients who underwent right-sided or left-sided hepatectomy was performed. In patients who underwent right-hepatectomy; liver failure was the primary cause of mortality with significantly decreased mortality observed in patients with preoperative biliary drainage. In patients who underwent left-hepatectomy, sepsis was the primary cause of mortality with significantly increased mortality observed in patients with preoperative biliary drainage.

Other authors recommend PBD of the FLR prior to hepatectomy only when a small anticipated FLR is expected, < 30%.[46] [58] In a smaller review of 60 patients who underwent hepatic resection for cholangiocarcinoma, 21 patients had a FLR of less than 30%. Of these 21 patients, nine had PBD of the FLR while 12 did not. Preoperative biliary drainage of patients with a small FLR was associated with significantly few deaths and hepatic insufficiency; no such difference was observed in the 39 patients with a FLR above 30%.[49]

Recommendations

Preoperative biliary drainage is not routinely recommended for patients with mid- to low- obstructions without cholangitis or malnutrition. In patients with high biliary obstructions undergoing hepatectomy with a small anticipated FLR there may be a role for routine PBD of the FLR to decrease the risk of hepatic insufficiency.

Transjugular Intrahepatic Portosystemic Shunt

The role of transjugular intrahepatic portosystemic shunt (TIPS) for variceal bleeding, either as rescue therapy or as an early intervention for patients at high-risk for treatment failure, has been established.[59] [60] [61] TIPS for refractory ascites has also demonstrated superiority compared with large volume paracentesis with albumin suplementation.[62] [63] Patients awaiting liver transplantation often suffer from the above conditions, with TIPS creation not a contraindication to subsequent transplantation. Ensuring an uneventful portal vein anastomosis at surgery is a goal when measuring for TIPS placement in these patients, as complications have been observed when the stent extends into the inferior vena cava (IVC) or proximal main PV.[64] In a series of 61 patients who went onto transplantation after TIPS, prolonged surgery related to TIPS migration was observed in 28% of patients.[65]

There has been recent interest in an emerging role for TIPS to treat and prevent portal vein thrombosis (PVT) propagation prior to liver transplant.[66] [67] [68]

Portal vein thrombosis is a common finding in the setting of cirrhosis, diagnosed before liver transplant on preoperative imaging studies or intraoperatively at rates between 5 to 26%.[69] The presence and degree of PVT has been shown to add to the technical difficulty of transplantation, increased hospital readmission rates, as well as increased morbidity and mortality.[70] [71] [72] [73] A large series reported preoperative PVT to be associated with a 50% increase in 1-year mortality, regardless of MELD score.[74] Fortunately, nonocclusive PVT is more common than occlusive PVT that extends into the splenic or superior mesenteric veins. To prevent the propagation of clot to this point, some investigators have advocated for TIPS to prevent propagation and induce recanalization of the portal vein.[73] [75] [76] The risk of bleeding in patients with portal hypertension, however, is a concern.

Transjugular intrahepatic portosystemic shunt is an alternate method to prevent propagation of PVT and induce recanalization. This method acts by decreasing intrahepatic vascular resistance and increasing portal blood flow, factors directly related to the development of PVT in the setting of cirrhosis.[77] [78]

Transjugular intrahepatic portosystemic shunt has been performed in the setting of PVT for the past 20 years, with technical success dependent on the degree and chronicity of thrombosis and replacement of the native portal vein with a fibrotic cord.[79] [80] Operator experience is critical as well, as a transhepatic or transsplenic approach may be necessary to achieve technical success depending on the nature of PVT.[79] [81] If needed, a variety of endovascular tools is available to establish patency, including balloon angioplasty, catheter-directed thrombolysis with tissue plasminogen activator (tPa; Genentech, San Francisco, CA), mechanical thrombectomy (Fogarty thrombectomy; Edwards Life Sciences, Irvine, CA), or pharmacomechanical thrombectomy (Angiojet; Possis Medical, Minneapolis, MN).

Initial studies that investigated TIPS performed with bare-metal stents demonstrated low patency rates and high rates or obstruction that required close follow-up and invasive revisions.[82] [83] Since the introduction of covered stent-grafts designed to reduce bile-leakage and intimal hyperplasia, improved patency rates have been observed.[84] [85] [86]

An initial review of TIPS for PVT in nine patients was successful at maintaining PV patency in eight of nine patients, with two patients undergoing liver transplant with patent portal veins and three more awaiting transplant with patent portal veins.[66] A more recent retrospective review compared 15 patients with partial PVT who underwent TIPS before liver transplant to eight patients with partial PVT who received liver transplant without TIPS.[67] Clinical characteristics were similar between the two groups. At time of liver transplant, the portal vein was patent in all patients who received TIPS, but completely occluded in half of the patients who did not undergo TIPS, a statistically significant difference. No significant difference in transfusion requirement, ischemia, or technical complications was observed between the two groups.

In the largest review of 70 patients who received TIPS in the setting of PVT, TIPS resulted in a completely recanalized PV, decreased PVT, and no improvement in PVT in 57%, 30%, and 13% of patients, respectively.[68] Of those with complete resolution of PVT, only two had recurrence of PVT. During follow-up, 15 patients went onto liver transplant while 15 remained listed for liver transplant. Ten patients died during follow-up, 28 were not listed due to stable disease, and two were lost to follow-up.

Although technical success rates are high, the procedure is not without complications. The rate of covered TIPS dysfunction at 1 and 2 years was 21% and 29%, similar to other studies.[69] [80] [86] The occurrence of hepatic encephalopathy after TIPS also remains a concern, with observed rates between 16 and 58%.[87] In the preoperative patient, stent migration is a concern as migration may complicate liver transplantation. Reported rates of stent migration vary between series with rates between 0 and 28%.[65] [67] [88] Other complications including hemoperitoneum, sepsis, aspiration, and spontaneous bacterial peritonitis are relatively rare.

The effectiveness of TIPS at reversing of halting PVT must be balanced against the known complications and improving surgical techniques at dealing with PVT intraoperatively. In a report of liver transplant in 32 patients with PVT, surgical thrombectomy was successful in 96% of patients. The one failure in this series was a case of PVT that involved both the superior mesenteric vein (SMV) and splenic vein (SV).[72] A more recent review of the liver transplant experience in the setting of PVT suggested that survival is similar between those with and without PVT when an anatomical end-to-end portal anastomosis is possible.[69] When a more complex anastomosis is required, however, 1- and 5-year survival rates decrease.[89]

Direct Intrahepatic Portocaval Shunt

The creation of a direct intrahepatic portocaval shunt (DIPS) was first described over a decade ago.[90] This technique involves an intravascular ultrasound- (introduced via a transfemoral approach) guided puncture (introduced via a transjugular approach) from the IVC through the caudate lobe of the liver into the portal vein. This technique is most commonly performed for the same clinical indications as the TIPS procedure, variceal bleeding, and ascites. Advocates of this technique state that DIPS benefits from higher primary patency rates because placement of the proximal end of the stent in the IVC avoids stent dysfunction secondary to hepatic vein stenosis.[91] Direct intrahepatic portocaval shunt procedure may also be safer because blind portal vein punctures are avoided, although lower complications rates have not been proven.[92] Although DIPS in the setting of portal vein thrombosis has not been widely described, ultrasound guidance could theoretically increase the technical ease of shunt creation while preserving the benefits of lowering intrahepatic vascular resistance and increasing portal blood flow.

Contraindications to TIPS/DIPS include congestive heart failure and severe primary hypertension.[93] After TIPS/DIPS, an exacerbation of hepatic encephalopathy may be observed and should be carefully assessed for.

Recommendations

Transjugular intrahepatic portosystemic shunt for recurrent variceal bleed or ascites in patients who go on to eventual transplantation is well established. Care to not extend the stent into the IVC or proximal main PV can decrease the chance of a complicated transplantation.

The goal when managing patients with PVT prior to liver transplantation is to allow for a conventional end-to-end anastomosis at surgery. Anticoagulation and TIPS have both demonstrated effectiveness at PV recanalization and prevention of PVT propagation. Clinical aspects of a given case and technical experience for dealing with PVT intraoperatively will determine which treatment, if any, is appropriate.

Direct intrahepatic portocaval shunt prior to liver transplantation has not been reported, although increased operative times have been observed in patients with a TIPS stent that extends into the IVC.

Balloon-Occluded Retrograde Transvenous Obliteration of Gastric Varices

Bleeding gastric varices (GV) are often managed initially with endoscopic banding or the administration of sclerosants. Rebleeding after endoscopic therapy, however, is a common occurrence.[94] Should rebleeding occur, spontaneous shunts, most often splenorenal or gastrorenal, allow for percutaneous treatment with balloon-occluded retrograde transvenous obliteration (BRTO).[95] This procedure was first reported over two decades ago, but until recently, was performed almost exclusively in Asia.[96]

Indications for BRTO include bleeding GV, GV with encephalopathy, and GV with ascites. In patients with GV and ascites, BRTO may be performed before, during, or after TIPS depending on the clinical scenario. As GV have a greater tendency to bleed at low portal pressures (< 12 mm Hg), Transjugular intrahepatic portosystemic shunt may treat the ascites without treating the GV.[97] This requires the addition of BRTO to the treatment of these patients.

Preoperative imaging before BRTO is critical to identify the portosystemic shunt necessary to perform the procedure. The technical aspects of BRTO have been previously described in detail.[98] [99] Briefly, access to the systemic venous system is obtained via a transjugular or transfemoral approach. A compliant balloon is positioned at the systemic side of the shunt and inflated. A venogram is then performed to assess the anatomy of the varices, with collateral vessels identified and occluded to prevent nontarget embolization and sclerosant dilution. Then, the sclerosant of choice (ethanolamine oleate, polidocanol, sodium tetradecyl sulfate) is injected into the varices via a microcatheter advanced through the occlusion balloon. The balloon is left inflated for a variable period, often around 3 hours. Repeat venography may then be performed to assess for satisfactory sclerosis. Good clinical results have been observed with BRTO, with GV obliteration rates between 80 to 100% and rebleeding rates less than 15%.[95] Worsening of esophageal varices, however, has been observed after BRTO and may require subsequent treatment.

Recommendations

Endoscopic management of bleeding gastric varices is typically regarded as first-line therapy. In patients with recurrent bleeding, BRTO is a safe and effective minimally invasive technique, particularly in patients with hepatic encephalopathy or contraindications to TIPS.

Postoperative Roles

Management of Postoperative Biliary Complications

Biliary leaks and strictures are known complications that may be seen after hepatic resection or transplantation and can lead to peritonitis or sepsis.[100] [101] Endoscopic management is the treatment of choice, but may be technically difficult or impossible depending on postsurgical anatomy.[102] [103]

Percutaneous Dilatation of Biliary Strictures

Biliary strictures after liver transplantation often occur within 4 months, occurring either at the anastomosis or in a separate area of ischemia.[102] This can be treated endoscopically with balloon dilatation and stenting or surgically with anastomotic revision. Indications for percutaneous biliary intervention include technically unsuccessful endoscopy due to anatomy or a low stenosis and stricture in a patient that is not suitable for open surgical revision.

Percutaneous puncture of the biliary system is performed with ultrasound and fluoroscopic guidance. Once access is obtained, a hydrophilic wire is used to cross the stenosis. Balloon-dilatation can be performed and an internal–external drain is then advanced across the stricture. The patient returns every several weeks to exchange the catheter for a larger size to slowly dilate the stenosis. This procedure is not optimal, as the external drain is prone to infection. Furthermore, the patient's quality of life is decreased having to live with an external drain for several months. More recently, cutting balloons and removable stents have been used with promising results.[104] [105]

Percutaneous biliary dilatation has demonstrated clinical utility in patients with postsurgical anatomy that does not permit endoscopic intervention or in whom endoscopy has failed. A review of 83 patients with stricture after liver transplant with a hepaticojejunostomy found excellent 1- and 3-year patency rates of 95 and 81% after percutaneous serial dilatation.[106] In another review of posttransplant patients treated percutaneously after failed endoscopy, a success rate of 87% was observed.[107] These high success rates are not universal, as other studies reported restenosis in as many as 58% of patients after percutaneous biliary dilatation.[108] [109]

After failed balloon dilatation or serial drainage, retrievable covered biliary stents deployed percutaneously have demonstrated clinical utility in 32 patients with benign strictures, 14 posttransplant. Primary patency and clinical success rates of 90 and 97% were observed in these patients.[105] A liver transplant patient with a biliary stricture that failed serial dilatation, eventually requiring stent placement, is presented in [Fig. 3]. A larger comparison of 66 patients who received percutaneous balloon dilatation or temporary stenting demonstrated shorter indwelling catheter times and a primary patency rates of 87% at 3 years with removable stents. Only two of 35 stents migrated while one of 35 stents was not successfully removed percutaneously.[110]

Recommendations

Percutaneous biliary dilatation is effective for the treatment of postoperative biliary strictures when surgery or endoscopy is not possible or unsuccessful. The use of removable covered stents is promising, as higher patency rates and shorter indwelling catheter times have been observed.

Percutaneous Biliary Diversion for Postoperative Biliary Leak

Biliary leak is a known complication after hepatic resection, the incidence of which is dependent on several factors. A large cut surface, increased operative blood loss, longer operative time, concomitant hepaticojejunostomy, and resection of a peripheral cholangiocarcinoma or segment 4 have all been associated with increased risk for biliary leak.[111] Currently, nonsurgical management is the preferred approach for the majority of bile leaks. In fact, drain retention or drain salvage is often sufficient.[112] For intractable bile leaks, endoscopic or percutaneous approaches are then considered with surgical exploration used when less-invasive methods fail.

Percutaneous puncture of a nondilated system in the setting of a biliary leak is technically more difficult than puncturing a dilated system. Higher rates of complications have been reported, as a more central puncture is often needed.[113] This technical difficulty may necessitate T-drainage, additional CT-guided punctures, or temporary gallbladder drainage to achieve technical success.[114] After access is obtained, external drainage is established proximal to the area of leak or internal–external drainage can be obtained to bridge the leak. Alternatively, removable covered stents have been deployed across bile leaks in a small series with no recurrence at one year.[115]

In the setting of major bile duct injuries like complete transection, a “rendezvous” procedure can be performed by the interventional radiologist and gastroenterologist. A wire is first passed endoscopically into the subhepatic space and then snared percutaneously. An internal–external drain is than placed, followed by a contralateral percutaneous biliary drain. These drains can then be exchanged for stents that are later removed.[116]

The effectiveness of percutaneous drainage for the management of postoperative biliary leaks is well established with success rates between 80 and 91%.[117] [118] [119] [120] Length of time needed for drainage varies widely between patients, but is usually in the range of several weeks. Clinical experience with the rendezvous technique has also been good, with this combined approach avoiding surgery in 20 of 22 patients.[116] Complications after percutaneous biliary drainage vary between studies, but one of the largest reviews demonstrated overall (14.5% vs. 6.9%) and major (8.4 vs. 2.1%) complication rates to be higher in patients with nondilated biliary systems compared with those with dilated systems.[113] Bleeding requiring transfusion and sepsis were the most common major complications in these patients.

Recommendations

Percutaneous biliary drainage is effective at managing intractable bile leaks in the postoperative setting and often avoids the need for surgical revision.

Management of Posttransplant Arterial Complications

Hepatic Artery Stenosis

The spectrum of postoperative vascular complications includes stenosis or thrombosis of the hepatic artery. Hepatic artery stenosis occurs in 4 to 11% of patients and can lead to eventual thrombosis, biliary ischemia, and graft dysfunction.[121]

Hepatic artery stenosis has been treated with balloon angioplasty, bare-metal stents, and drug-eluting stents. Long-segment stenosis or kinking and tortuosity of the hepatic artery has been reported to limit the success of balloon angioplasty.[122]

A large meta-analysis that investigated balloon angioplasty and stent placement for hepatic artery stenosis demonstrated high technical success rates of 90 and 98% and long-term patency rates of 76 and 68%.[123] Of the 147 patients treated with balloon angioplasty and 116 patients treated with stents, retransplantation was needed in 16 and 11 patients, respectively. Reported complication rates are low, generally less than 10%.[123]

Hepatic Artery Thrombolysis

Intra-arterial thrombolysis (IAT) is an endovascular option for patients with hepatic artery thrombosis. However, the use of thrombolysis in the immediate postoperative setting can lead to life-threatening bleeding and caution in this setting is warranted. This concern combined with the questioned clinical efficacy of revascularization for late thrombosis has led some authors to suggest a narrow window for safe and effective endovascular treatment for hepatic artery thrombosis.[124]

A large review of 69 patients reported in 16 cases examined intra-arterial thrombolysis with urokinase, tPa, and streptokinase infused continuously or by bolus for hepatic thrombosis. Intra-arterial thrombolysis was successful in 47 of 69 patients, with 62% of these patients requiring repeat intervention.[125] In this study, hemorrhage was seen in 18 patients, with bleeding being fatal in three patients. Less common complications include dissection, thrombosis, or rupture of the hepatic artery.

Recommendation

Endoluminal treatment of hepatic artery stenosis has high technical success and patency rates, although this impact on long-term graft function is not established. The experience with intra-arterial thrombolysis for hepatic artery thrombosis is limited. The benefits of a minimally invasive treatment must be balanced against relatively high rates of technical failure and the risk of bleeding in the immediate postoperative setting.

Management of Posttransplant Venous Complications

Stenosis of the IVC, portal vein, or hepatic veins occurs less commonly than arterial complications.[126] [127] [128] The clinical presentation may include portal hypertension, ascites, pleural effusions, lower extremity edema, and graft failure. Percutaneous intervention is the first-line treatment because of its high success rates and low rates of complication.[129] Intervention is performed by a transjugular approach for an outflow stenosis or by a transhepatic approach for portal vein stenosis. As a transhepatic puncture is needed for the treatment of a portal vein stenosis, higher complication rates are expected. A guidewire is used to cross the stenosis with pressure measurements performed to confirm a hemodynamically significant stenosis. Balloon angioplasty is the preferred method of treatment, with repeat angioplasty often needed, but producing excellent clinical results.[130] Endovascular stents may be used for a stenosis not responsive to repeat angioplasty, with a lower threshold generally for stenting a portal vein and primary stenting advocated by some.[131] [132]

A venous stenosis is an uncommon complication after liver transplant that can cause significant symptoms and graft dysfunction. Endovascular angioplasty with or without stenting is first-line treatment with high rates of technical and clinical success reported.

Conclusion

Interventional radiologists play a diverse and ever-changing role in the multidisciplinary management of the patients with a liver lesion in both the pre- and postoperative setting. A multidisciplinary approach is necessary to coordinate and facilitate the appropriate care that these patients need in a timely manner.

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Address for correspondence

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