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DOI:10.2214/AJR.05.1250
AJR 2007; 188:659-664
© American Roentgen Ray Society

Clinical Observations

Endovascular Shunt Reduction in the Management of Transjugular Portosystemic Shunt-Induced Hepatic Encephalopathy: Preliminary Experience with Reduction Stents and Stent-Grafts

Geert Maleux1, Chris Verslype2, Sam Heye1, Guido Wilms1, Guy Marchal1 and Frederik Nevens2

1 Department of Radiology, University Hospitals Gasthuisberg, Herestraat 49, Leuven, Belgium, B/3000.
2 Department of Hepatology, University Hospitals Gasthuisberg, Leuven, Belgium, B/3000.

Received July 19, 2005; accepted after revision October 10, 2005.

 
Address correspondence to G. Maleux (geert.maleux{at}uz.kuleuven.ac.be).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to retrospectively evaluate the safety, feasibility, and midterm clinical outcome of the use of three types of reduction stents inserted to manage transjugular intrahepatic portosystemic shunt (TIPS)-induced hepatic encephalopathy refractory to medical treatment.

CONCLUSION. The use of a covered reduction stent-graft results in a greater increase in portosystemic gradient immediately after reduction than does use of a bare reduction stent. Relief of TIPS-induced hepatic encephalopathy tends to be greater in patients with reduction stent-grafts than in those with bare reduction stents.

Keywords: grafts • implantable devices • interventional radiology • liver disease • vascular stents


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Hepatic encephalopathy (HE) is a known complication that develops after creation of a transjugular intrahepatic portosystemic shunt (TIPS) [1, 2]. HE classically is characterized by neuropsychiatric symptoms, such as impaired performance of addition, disorientation to time and place, lethargy, and apathy, and can become life-threatening with the development of gross dis-orientation, somnolence, and even coma [3, 4]. New or worsened HE after TIPS placement has been reported to occur in 5-47% of patients [5, 6]. In most patients, however, conservative medical therapy, essentially administration of lactulose and nonabsorbable antibiotics to reduce the nitrogenous load from the intestine, can successfully control this condition. In 3-7% of patients, however, HE remains refractory to medical treatment, and further invasive treatment is mandatory. Although liver transplantation is the best option, various interventional techniques have been described for reducing shunt diameter to decrease or eliminate TIPS-induced HE [5, 7-10]. The purpose of this study was to evaluate the radiologic, hemodynamic, and clinical performance of three types of self-expanding reduction stents: constraining bare stents, constraining polyurethane-covered stent-grafts, and constraining expanded polytetrafluoroethylene (e-PTFE)-covered stent-grafts.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Selection
No specific approval by our institutional review board is needed for retrospective studies. Informed consent was obtained from all patients before the initial TIPS procedure and before the shunt reduction procedure. Between September 1992 and February 2005, 266 patients underwent TIPS procedures at our institution. The main indications for TIPS procedures at our institution are complications of portal hypertension refractory to medical or endoscopic therapy, generally endoscopically uncontrollable variceal bleeding, recurrent variceal bleeding despite endoscopic therapy, refractory ascites, and refractory hepatic hydrothorax. No patient with a Child-Pugh score worse than C12 was referred for TIPS. We usually try to obtain a final portosystemic gradient of 12 mm Hg or less, and therefore all shunts are balloon dilated up to 8-10 mm in diameter.

Sixteen (6%) of the 266 patients (four women, 12 men; mean ± SD age, 60 ± 10.8 years; age range, 35-80 years) presented with debilitating clinical signs of TIPS-induced HE unresponsive to classic medical therapy. Medical treatment consisted of increased dietary fiber intake and administration of lactulose (Bifiteral, Solvay Pharma) and an antibiotic cocktail of neomycin, metronidazole, and amoxicillin. The underlying hepatic disease was alcoholic liver cirrhosis (n = 11), hepatitis C cirrhosis (n =2), autoimmune hepatitis (n = 1), toxic (methotrexate) hepatitis (n = 1), and cryptogenic liver cirrhosis (n = 1). The Child-Pugh scores were A (n =2), B (n =13), and C (n = 1). Stents placed during the initial TIPS procedure were Wallstents (Boston Scientific) (n =5), Memotherm stents (Angiomed) (n =2), and Viatorr stent-grafts (W. L. Gore & Associates) (n = 9). All these stents were postdilated to a shunt diameter of 8-10 mm. The indication for initial TIPS was variceal bleeding (n = 10 [62.5%]) or refractory ascites (n = 6 [37.5%]). Clinical assessment of HE despite therapy was made in accordance with the West Haven criteria for semiquantitative grading of mental state. The findings were grade 4 (n =7), grade 3 (n = 6), and grade 2 (n = 3). Clinical evidence of refractory HE was found and percutaneous shunt reduction was scheduled a mean of 9.5 months (range, 0-42 months) after the initial TIPS procedure.


Figure 1
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  		Fig. 1A —35-year-old woman (patient 1) who received a transjugular intrahepatic portosystemic shunt for ascites and 3 months later had recurrent episodes of comatose state due to hepatic encephalopathy. Portogram shows portosystemic shunt with Wallstent (Boston Scientific) inserted for refractory ascites.

 


Figure 2
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  		Fig. 1B —35-year-old woman (patient 1) who received a transjugular intrahepatic portosystemic shunt for ascites and 3 months later had recurrent episodes of comatose state due to hepatic encephalopathy. Photograph shows Memotherm reduction stent (Angiomed) used to manage hepatic encephalopathy. Narrowest part (arrow) of reduction stent (arrowheads) was 5 mm in diameter.

 


Figure 3
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  		Fig. 1C —35-year-old woman (patient 1) who received a transjugular intrahepatic portosystemic shunt for ascites and 3 months later had recurrent episodes of comatose state due to hepatic encephalopathy. Radiograph shows Memotherm reduction stent (arrowheads) within Wallstent shunt. Narrowest part of reduction stent (arrow) was 5 mm in diameter.

 


Figure 4
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  		Fig. 1D —35-year-old woman (patient 1) who received a transjugular intrahepatic portosystemic shunt for ascites and 3 months later had recurrent episodes of comatose state due to hepatic encephalopathy. Completion portogram after reduction shows no angiographic reduction of shunt although reduction stent (arrowheads) is in place and narrowest part of stent (arrow) is 5 mm in diameter. There was no difference in portosystemic pressure gradient before and after shunt reduction.

 
TIPS Reduction Procedure
Shunt reduction procedures were performed via the right jugular approach in 13 patients under local anesthesia (lidocaine hydrochloride; Xylocaine, AstraZeneca). In the other three patients, the procedure was performed under general anesthesia because the patients had been reintubated after the initial TIPS procedure because of their prolonged comatose state.

After placement of a 12-French sheath (Check-Flo introducer set, Cook), pressure measurements were obtained from the inferior vena cava (at the level of the hepatic segment) and the portal vein. The mean portosystemic gradient before shunt reduction was 6 ± 2.5 (SD) mm Hg (range, 3-10 mm Hg). In all cases, direct portography showed a fully patent shunt without evidence of focal shunt stenosis. After exchange for a stiff guidewire (Amplatz, Cook), the reduction stent was placed over the parenchymal track of the initial TIPS stent in order not to cover portal vein branches.

Six patients received a self-expanding nitinol reduction stent with a net of polyethylene terephthalate thread outside the narrow part (Memotherm reduction stent) (Fig. 1A, 1B, 1C, 1D). This type of reduction stent is not available in the United States and is no longer available in Europe. In the other 10 patients, covered stent-grafts were inserted. Four patients received a self-expanding polyurethane-covered reduction stent-graft (OptiMed reduction stent-graft, OptiMed) (Fig. 2A, 2B, 2C), and six received a modified covered reduction stent-graft with a Memotherm reduction stent in which a Viatorr stent-graft was deployed (Fig. 3A, 3B, 3C). The last technique has been used since the Viatorr stent-graft became commercially available in Europe at the end of 2000. The narrow part of all reduction stent-grafts had an internal diameter of 5 mm. Completion portography was performed and portosystemic pressure measurements were repeated after insertion of the reduction stent. In case of reopacification of fundal or esophageal varices, prophylactic coil (0.035 MReye, Cook) embolization was performed. Patients were discharged depending on their overall clinical state. No analgesic or anticoagulation therapy was administered during or after the procedure.


Figure 5
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  		Fig. 2A —68-year-old man (patient 10) who underwent transjugular intrahepatic portosystemic shunt (TIPS) placement because of refractory ascites and then shunt reduction because of multiple episodes of stupor and unconsciousness. Portogram shows Viatorr stent-graft (W. L. Gore and Associates) used for TIPS.

 

Figure 6
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  		Fig. 2B —68-year-old man (patient 10) who underwent transjugular intrahepatic portosystemic shunt (TIPS) placement because of refractory ascites and then shunt reduction because of multiple episodes of stupor and unconsciousness. Photograph shows self-expanding OptiMed reduction stent-graft with narrowest (5-mm) diameter (arrow) within shunt.

 

Figure 7
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  		Fig. 2C —68-year-old man (patient 10) who underwent transjugular intrahepatic portosystemic shunt (TIPS) placement because of refractory ascites and then shunt reduction because of multiple episodes of stupor and unconsciousness. Portogram shows shunt placement resulting in reopacification of intrahepatic portal veins and clear reduction of shunt diameter in narrow segment (arrow) of reduction stent-graft.

 

Figure 8
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  		Fig. 3A —58-year-old man (patient 11) who underwent emergency transjugular intrahepatic portosystemic shunt (TIPS) procedure because of variceal bleeding unresponsive to pharmacologic and endoscopic treatment. One month after TIPS procedure, patient became stuporous and was treated with reduction stent. Portogram shows TIPS.

 

Figure 9
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  		Fig. 3B —58-year-old man (patient 11) who underwent emergency transjugular intrahepatic portosystemic shunt (TIPS) procedure because of variceal bleeding unresponsive to pharmacologic and endoscopic treatment. One month after TIPS procedure, patient became stuporous and was treated with reduction stent. Photograph shows Memotherm reduction stent (Angiomed) relined with Viatorr stent-graft (W. L. Gore and Associates), which was centrally constrained to 5-mm diameter.

 

Figure 10
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  		Fig. 3C —58-year-old man (patient 11) who underwent emergency transjugular intrahepatic portosystemic shunt (TIPS) procedure because of variceal bleeding unresponsive to pharmacologic and endoscopic treatment. One month after TIPS procedure, patient became stuporous and was treated with reduction stent. Completion portogram shows antegrade reopacification of intrahepatic portal veins and clearly visible narrow segment (arrow) of portosystemic shunt. Coils (arrowheads) placed to occlude esophageal varices, which reopacified immediately after shunt reduction, are evident.

 
Shunt Reduction Follow-up
Follow-up was done through analysis of medical records. At our institution every patient with a TIPS undergoes close follow-up by a member of the department of hepatology. Clinical and biochemical evaluation is routinely performed. Liver sonography is performed every 6 months and when recurrent symptoms of portal hypertension or other adverse events occur. Ammonium levels were not routinely assessed. Especially for patients with suspected HE, follow-up consisted of clinical evaluation with special attention to mental status in accordance with the West Haven criteria. Invasive venography and pressure measurements were performed in cases of persistent HE and in cases of recurrent complications of portal hypertension. Depending on the findings on venography, additional percutaneous interventions were performed.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Hemodynamic and Clinical Evolution
No procedural complications occurred during insertion of the reduction stents or stent-grafts. The technical characteristics of the shunt reduction procedures are summarized in Table 1. The portosystemic gradient before and immediately after shunt reduction for each patient is also shown in Table 1. The mean portosystemic gradients before and immediately after reduction were 4 and 7 mm Hg for the reduction stent group (n = 6) and 6 and 13 mm Hg for the stent-graft group (n =10) (Table 1). In five (31%) of the patients, reopacification of fundal or esophageal varices was found on completion portography after shunt reduction, and the varices were embolized by coil placement. Mental status assessment after shunt reduction, as described in Table 2, showed a decrease in or complete disappearance of HE in two of the six patients in the Memotherm reduction stent group and eight of the 10 patients in the reduction stent-graft group.


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  		TABLE 1: Technical Characteristics of Shunt-Reduction Procedures

 

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  		TABLE 2: Clinical and Radiologic Follow-Up Data

 

Endovascular Interventions During Follow-up
During follow-up, additional endovascular interventions were necessary in five (31%) of the patients. Patient 9, initially treated with an OptiMed reduction stent-graft, presented with recurrent symptoms of severe ascites 1 week after shunt reduction. Direct portography revealed increased luminal narrowing compared with the completion venographic findings immediately after insertion of the reduction stent-graft. A balloon-expandable stent (Corinthian PQ 394, Cordis Johnson & Johnson) mounted on a 7-mm balloon catheter (Smash, Boston Scientific) was placed to widen the narrowest part of the reduction stent-graft. The same patient presented with recurrent symptoms of ascites 5 months after the initial TIPS-reduction procedure. Invasive venography revealed tight stenosis of the distal end of the OptiMed reduction stent-graft. An additional stent-graft (Viatorr) was inserted, and the narrow part of the reduction stent-graft was dilated to 5-mm diameter. During follow-up, no recurrent stent-graft occlusion was detected.

Patient 7 presented with anemia, and recurrent esophageal varices were visualized at endoscopy 14 months after reduction stent-graft insertion. Invasive venography revealed shunt occlusion. After percutaneous recanalization, an additional bare stent (Memotherm Flexx, Angiomed) was placed in the previously occluded shunt, and the narrow part of the shunt was redilated up to 5 mm. Patient 10, also treated with insertion of an OptiMed reduction stent-graft, did not respond clinically to an increased portosystemic gradient after shunt reduction because of a persistent comatose state. Complete shunt occlusion was performed with the use of a balloon (Goldvalve, Nycomed). The patient's neuropsychiatric state normalized, but intractable ascites redeveloped. Orthotopic liver transplantation was performed 1.5 months after percutaneous shunt occlusion.

In the Memotherm plus Viatorr reduction stent-graft group, additional narrowing of the shunt was performed on patient 14 because of a persistent comatose state and in patient 16 because of residual signs of HE (grade 2; before initial reduction, grade 4). In these two cases additional shunt reduction was performed by placement of a self-expanding e-PTFE-covered stent-graft (Viatorr) within the previously reduced shunt. A balloon-expandable bare stent (Express, Boston Scientific) was dilated up to 7-mm diameter in parallel with and subsequently extrinsically constraining the diameter of the Viatorr stent-graft to a residual diameter of 3 mm as previously described by Saket et al. [8]. In one patient additional shunt reduction resulted in a further decrease of HE from grade 2 to grade 1. The other patient did not have good clinical results and died of a combination of hepatic coma, terminal liver insufficiency, and multiple organ failure. During follow-up, eight patients received a constraining TIPS stent relined with an e-PTFE stent-graft. No early or late occlusion was found in these eight patients.

Overall Survival
The overall survival rate was 69%, 11 of 16 patients surviving. The mean follow-up period was 16.5 months (range 0.3-71 months). Three of the surviving patients (patients 1, 5, and 10) received definitive treatment with orthotopic liver transplantation. The mental status of the patients is shown in Table 2.


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
TIPS-induced HE in most cases responds well to conservative medical therapy. In only a small percentage (3-7%) of cases [7, 11], HE is refractory to conservative management consisting of administration of products, such as lactulose and nonabsorbable antibiotics, for reducing the nitrogenous load from the intestine [11]. In these cases of refractory HE, more invasive therapy is mandatory. Although liver transplantation is the best treatment, it is not always possible in due time. In addition, transplantation sometimes is not necessary, especially in patients with postalcoholic cirrhosis who have stopped drinking. Therefore, minimally invasive techniques are attractive, and several case reports [5, 8, 9] have described their usefulness.

The first percutaneous endovascular attempts to manage refractory HE induced by surgical shunts were permanent shunt occlusion with vascular coils or detachable balloons [12]. Despite clinical success, this technique was not free of morbidity or even mortality because definitive shunt occlusion potentially can induce variceal hemorrhage and it is not possible to easily reopen the shunt. Paz-Fumagalli et al. [13] described a case of death after shunt occlusion; sudden severe hemodynamic alterations caused decreased cardiac output, hypotension, and metabolic acidosis. A first attempt to deal with these limitations of shunt occlusion was the technique of reversible shunt occlusion described by Kerlan et al. [14] and Haskal et al. [10]. Placement of a latex occlusion balloon in the shunt for 24 or 48 hours resulted in shunt thrombosis, but the ability to recanalize the occluded shunt afterward, if needed, was safeguarded. However, this technique was not free of potential complications, including variceal rebleeding and reestablishment of refractory ascites due to a marked increase in portal pressure, balloon migration to the right side of the heart, and clot migration to the pulmonary circulation.

Constraining stents and constraining stent-grafts have been used to reduce shunt diameter. These devices have the advantage of not completely occluding the shunt but only diminishing flow within the shunt by reducing shunt diameter. Different types of locally modified and commercially available reduction stents have been described in the literature. Haskal et al. [15] and Brophy and Haskal [16] used a Wallstent they constrained with a silk suture to make an hour-glass-shaped stent with a constraining diameter of 5 mm. Forauer and McLean [9] used a Palmaz stent (Cordis, Johnson & Johnson) that they anchored in the Wallstent with a braided polyglactin suture; the result was a constrained configuration of the Wallstent. Hauenstein et al. [7] described the first, to our knowledge, clinical experience of a commercially available self-expanding reducing stent. We used this stent in the first six patients in our study. All these constraining stents can cause turbulence in the shunt lumen, which can increase the portosystemic pressure gradient and narrow the true shunt lumen. Hauenstein et al. found clinical improvement in mental state in four of seven patients with TIPS-induced HE. In our study, we observed clear clinical benefit in only two of six patients treated with a Memotherm reduction stent. The reasons for limited success with this technique were lack of adequate elevation in portal pressure immediately after insertion of a reducing stent (mean, 3 mm Hg) and uncertainty about thrombus formation in the dead space between the narrow part of the reducing stent and the initial TIPS stent. Therefore, embolizing the dead space with coils [8] or with an embolic emulsion, as described by Gerbes et al. [17], is a valuable alternative, but no substantial clinical data on this technique are available.

A simpler method of reducing a portosystemic shunt more effectively, immediately, and in a more controlled way is to use reducing stent-grafts. Varied techniques have been described for obtaining an hourglass-shaped stent-graft [18-20]. All these techniques result in immediate and clear reduction of the shunt diameter and in an immediate and clear increase in portosystemic pressure gradient. Madoff et al. [5] found an immediate mean increase in portosystemic gradient of 9.3 mm Hg after insertion of a silk-suture-reduced Wallgraft device (Boston Scientific). Clinical success was achieved in five of six patients. We found a more marked increase (mean, 7 mm Hg) in portosystemic gradient when reducing the shunt with a stent-graft than we did using a bare stent (mean, 3 mm Hg). In addition, insertion of reduction stent-grafts resulted in better neuropsychiatric outcome compared with that in patients treated with reduction bare stents. Eight of 10 patients treated with a reduction stent-graft had a clear decrease in or complete disappearance of HE, compared with two of six patients treated with a bare reduction stent.

Although both types of reducing stent-grafts, polyurethane covered and e-PTFE covered, are effective in achieving immediate and significant hemodynamic changes and clinical benefit, the polyurethane-covered reduction stent-graft has the important limitation of possible total shunt occlusion resulting in recurrent development of portal hypertension-related symptoms. No shunt occlusion was detected in the e-PTFE reduction stent-graft group or in the patient retreated with an e-PTFE-covered stent for management of recurrent stenosis in a polyurethane-covered reduction stent-graft. The high incidence of shunt occlusion in TIPS relined with polyurethane or similar covering in an experimental model in which a covered stent-graft was used has been described by Haskal and Brennecke [21] and by Otal et al. [22]. The low rate of shunt occlusion with relining with e-PTFE covering has been found in both experimental models [23, 24] and in clinical trials of the Viatorr stent-graft [6, 25]. We observed a difference in maintaining the exact shunt diameter when the shunt was relined with e-PTFE compared with shunts relined with polyurethane. The difference in patency was accentuated by the fact that one patient initially treated with a polyurethane-covered reduction stent-graft and presenting with shunt stenosis was successfully treated with percutaneous shunt recanalization and insertion of a constraining e-PTFE stent-graft. Similar findings were described by Haskal et al. [19], who used an e-PTFE covered stent-graft to manage an occluded portosystemic shunt previously made with a Wallgraft device.

In conclusion, we found that reduction stent-grafts tend to be superior to bare reduction stents in achieving an immediate significant increase in portosystemic gradient by constraining the shunt diameter. Decrease in or complete disappearance of TIPS-induced HE is more frequently depicted after insertion of a reduction stent-graft than after use of a bare reduction stent. Our results also suggest that e-PTFE-covered reduction stent-grafts are superior to polyurethane-covered stents in maintaining the correct reduced shunt diameter without early or late shunt occlusion. On the basis of our preliminary experience with three types of reduction stents, we recommend insertion of an e-PTFE-covered reduction stent-graft as the most efficient interventional tool for managing TIPS-induced HE refractory to medical treatment.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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