What Is Known
- Transjugular intrahepatic portosystemic shunting is technically feasible in children.
- It is an effective management option for variceal bleeding and ascites, in children with portal hypertension, both pre- and post-liver transplant.
What Is New
- Transjugular intrahepatic portosystemic shunting may offer long-term treatment of portal hypertension and its complications; reducing the need to transplant in childhood.
- Complications following transjugular intrahepatic portosystemic shunting may be severe, including medically refractory encephalopathy or vascular injury necessitating early re-listing for transplantation.
- Most cases of stent stenosis are asymptomatic and so careful shunt surveillance is required long-term.
The aetiology of childhood portal hypertension (PHTN) differs from adults, and non-cirrhotic causes are more common. Adult studies demonstrate that variceal haemorrhage may occur once the hepatic venous pressure gradient is >12 mmHg. Although the mortality rate in children is low at the time of first bleed (1), bleeding causes death or necessitates emergency liver transplantation in up to 19% of those with large varices (2).
There are no UK guidelines for the management of paediatric PHTN. Ascites may be managed by sodium and fluid restriction, diuretics and, in refractory cases, albumin infusions and paracentesis (3). Endoscopic band ligation (EBL) is the first-line secondary prophylaxis for variceal bleeding (1,4). A transjugular intrahepatic portosystemic shunt (TIPSS) should be considered in children with variceal bleeding that has an intrahepatic aetiology, and which cannot be controlled endoscopically (5).
TIPSS is an interventional radiology procedure where a shunt is established between the portal vein (PV) and hepatic vein (HV) to decompress the portal venous system. In adults, the procedure is considered successful if the portosystemic gradient (PSG) falls to <12 mmHg (6). TIPSS has an established role in the management of adult PHTN (7,8), providing an effective portosystemic shunt without the morbidity and mortality associated with surgical shunts (9). There is, however, a paucity of evidence for its use in children (10–15). This study was undertaken to review our 20-year experience with TIPSS in children.
Methods are available online as Supplemental Digital Content (http://links.lww.com/MPG/B369) (16–18).
Forty children (20 boys, 20 girls) underwent TIPSS procedures. Two children each had 2 attempts, resulting in 42 attempted TIPSS procedures. Median age at time of TIPSS was 12 years (range 7 months–17 years) and median weight was 36 kg (range 6.4–78 kg).
There were a wide range of underlying causes of PHTN with the commonest being biliary atresia (n = 12, 30%) and cystic fibrosis-associated liver disease (n = 8, 20%). Three children had previously undergone liver transplantation; with either isolated whole-graft liver transplantation (n = 2) or combined reduced liver and small bowel transplantation (n = 1; Table 1).
All children had symptomatic PHTN resistant to conventional treatment. Thirty-five children (88%) had variceal bleeding that was not adequately controlled with an EBL programme due to ongoing active bleeding, >1 episode of breakthrough bleeding, or failure to ablate varices after 4 endoscopic sessions. Five of these children were on a non-selective beta-blocker. In children with intestinal failure-associated liver disease, varices were stomal (n = 3) or at the junction between the native duodenum and graft jejunum (n = 1). Four children had refractory ascites (10%) with respiratory compromise requiring drain insertion (n = 3) or daily albumin infusions (n = 1). One child (2%) had hypersplenism and paraspinal varices that precluded planned spinal surgery. Nineteen children had undergone liver transplantation assessment; 8 of these children were medically unfit for transplantation due to uncontrolled variceal bleeding.
Most children were Child-Pugh score A (n = 21, 57%), 10 scored B (27%) and 6 scored C (16%). Pre-operative paediatric end-stage liver disease (PELD)/model for end-stage liver disease (MELD) scores were mostly <10 (n = 20, 54%), 13 were 10–20 (35%) and 4 were >20 (11%). In 3 children scores were not known.
All TIPSS procedures were performed under general anaesthesia with intravenous antibiotic cover, by 1 of 4 interventional radiologists. Most procedures were elective (n = 34, 81%). Eight procedures (19%) were performed as an emergency due to active, life-threatening variceal bleeding. Blood products were transfused to children with a prothrombin time of >15 seconds or a platelet count of <80 × 109/L.
The HV was accessed via an internal jugular vein (IJV) under ultrasound guidance. The right IJV was catheterised preferentially (n = 39, 93%). The left IJV was used where the RIJV was occluded (n = 3).
The HV was catheterised using the Rosch-Uchida or Ring transjugular access system (Cook Medical, Bloomington, IN, USA) under fluoroscopy guidance (Fig. 1A). The right (n = 19, 45%), middle (n = 16, 38%), or left HV (n = 4, 10%) was catheterised. In the other 3 patients (7%), the track was created directly from the HV-IVC confluence to the portal venous system.
The PV was catheterised under fluoroscopic guidance (Fig. 1B). Intra-operative transabdominal ultrasound was used to identify the position of the PV and aid catheterisation (n = 19), as previously described (19). Some patients also required insertion of a guidewire into the PV (n = 13); superior mesenteric angiography (n = 4); or wedged portal venography (n = 4) to aid PV catheterisation. The TIPSS was created between the HV and the right (n = 22), left (n = 7), or main (n = 4) PV.
Following successful PV catheterisation, the track was balloon dilated before stent insertion. Between February 1995 and April 2000, the TIPSS was established with a self-expanding uncovered endoprosthesis (Wallstent; Schneider (Europe) AG, Bulach, Switzerland). A covered endoprosthesis (Viatorr; WL Gore & Associates (UK) Ltd, Livingston, UK) was initially deployed in February 2000, and has been used in all cases since April 2000. A single, 7 to 10 mm diameter stent was used in most cases (n = 21, 64%). In 12 cases (36%), 2 overlapping stents were inserted to ensure complete stenting from the main PV to the HV-IVC confluence (Fig. 1C). An additional stent was inserted to manage acute PV thrombosis (n = 1) or SMV-splenic vein stenosis (n = 1). Following insertion, the stent was balloon dilated to an internal diameter of 6 mm (n = 1), 8 mm (n = 23), or 10 mm (n = 7). Final internal diameter was not recorded in 2 cases.
The median operating time was 156 minutes (range 68–300 minutes). The median screening time was 42 minutes (range 10–88 minutes). The median radiation dose since 2010 (n = 14) was 6.7 mSv (range 1.3–16.0 mSv).
Post-operatively children were monitored clinically for evidence of encephalopathy, electroencephalography was performed, if suspected. Formal psychological evaluation was completed if there was concern regarding subclinical encephalopathy affecting behaviour or school performance.
Anticoagulant or antiplatelet therapy post-TIPSS was decided on a case-by-case basis. All children with Budd-Chiari syndrome (n = 3) were treated with lifelong warfarin, aiming for an INR of 2.0 to 3.0. One child received intravenous heparin until their death, 12 days post-TIPSS. Others received, dipyridamole (n = 7), aspirin and dipyridamole (n = 2), or warfarin (n = 1) for 1 year. Some patients were, however, not anticoagulated nor treated with antiplatelet therapy (n = 15). In 4 cases post-procedure anticoagulant therapy was not recorded.
Our post-operative TIPSS surveillance programme has changed over the study period. Currently, the TIPSS is evaluated with a 3-monthly ultrasound for the first year, followed by TIPSS venogram at 1 year and then annually. A TIPSS venogram is also performed if the ultrasound scan is abnormal or the child develops recurrent symptoms.
The TIPSS procedure was technically successful in 33 cases (79%), including in a 7-month-old, 6.4 kg infant (20). There were 9 technical failures, which were primarily due to abnormally small or disorganised PV anatomy (n = 4). In the remainder, the PV could not be cannulated, or a safe and stable position could not be established. Three cases had pre-operative imaging of the PV system with CT angiography (n = 2) or portal venography (n = 1), which showed vascular abnormalities that increased the risk of technical failure. In 2 patients, a repeated TIPSS attempt was successful.
Our technical success varied during the study (Fig. 2). Since October 2008, there has been an increased caseload, which has been accompanied by improved technical success. The current estimate of technical success is 82% (95% CI 62% to 93%). Univariate analysis did not identify any variables that were associated with technical success.
A technically successful TIPSS procedure was associated with a clinical improvement in almost all children. Bleeding stopped in 27 children (96%) with recurrent variceal haemorrhage. One child had persistent variceal bleeding post-TIPSS, which was not controlled with EBL and the patient died. In patients with refractory ascites, TIPSS led to resolution of ascites on ultrasonography in 3 children (75%), and a clinically relevant reduction in ascitic volume with resolution of respiratory compromise in the other one. In the child with hypersplenism, TIPSS resolved the paraspinal varices but splenic artery embolisation was required to treat the thrombocytopenia.
Comparative pre- and post-operative PV pressure data were available in 19 cases (58%). Post-TIPSS PV pressure reduced from 31 mmHg (range 12–42 mmHg) to 18 mmHg (range 9–24 mmHg) with a median PV pressure reduction of 10 mmHg (range −25 to +1 mmHg). Median PSG following the TIPSS procedure was 6 mmHg, (range 1 to 13 mmHg); 18 (95%) had a gradient <12 mmHg and 9 (47%) achieved a normal gradient (≤4 mmHg).
Native liver Survival
All UK patients have been followed up at a liver centre. One child from overseas was lost to follow-up at 12.6 years post-TIPSS. Median follow-up is 6.2 years (range 2.5–17.3 years). The 1-, 5-, and 10-year survival with native liver post-TIPSS was 57%, 35%, and 35%, respectively (Fig. 3A). Factors affecting actuarial survival with TIPSS included age and weight at TIPSS; and Child-Pugh and PELD/MELD scores. Multivariate analysis identified Child-Pugh score C as the only variable that independently increased risk of mortality, liver transplantation, or TIPSS failure (LR = 8.0; 95% CI 2.7 to 23.5; P = 0.001) (Fig. 3B).
Suitability for Transplantation
The TIPSS procedure was technically successful in 7 emergency cases (88%). These children were all unsuitable for transplantation due to haemodynamic instability. The clinical improvement enabled all to be listed for transplantation. In addition, 2 further children improved following TIPSS and were removed from the active transplant list. PHTN was the only indication for transplantation in both these cases.
Thirteen children underwent liver transplantation following a technically successful TIPSS procedure. Median time to transplantation was 340 days (range 2 days–2.4 years). In 4 cases, transplantation was made possible because of the haemodynamic improvement following TIPSS.
Seven children had previously undergone liver transplantation assessment. The TIPSS was performed as a bridge-to-transplantation. Median time from TIPSS to transplant in this sub-group was 93 days (range 2–612 days).
Twenty-five patients (76%) had comparative pre- and post-operative splenic measurements. Maximal splenic reduction was recorded at a median of 2.3 months post-TIPSS (range 3 days–4.9 years). Spleen size reduced from 16.3 cm (range 8.8–25 cm) to 14.3 cm (range 8.4–20.4 cm). Splenomegaly persisted in 24 cases (96%).
Six months post-TIPSS, thrombocytopenia resolved in 3 children. One child showed a more gradual improvement, achieving a normal platelet count 2 years post-TIPSS. All others (n = 25) remained thrombocytopenic until transplant, death, or the end of follow-up. There was no correlation between changes in platelet count or spleen size and any anatomical, pre-operative, or post-operative variable.
Nine children died with a patent TIPSS without undergoing liver transplantation. Median time to death was 74 days (range 12 days–15.8 years). Four children died within 30 days of TIPSS; 1 was unsuitable for transplantation and died of sepsis; 1 died from cerebral oedema on the active transplant waiting list having been unfit for transplantation pre-TIPSS; and 2 were initially listed for transplant post-TIPSS but were later suspended due to progressive disease and multiorgan failure. Septic events were unrelated to TIPSS.
Twenty-one children (64%) had a technically successful TIPSS without complication. Six children (18%) had a major complication. One child had hepatic artery (HA) thrombosis and liver infarction that caused severe sepsis and early re-transplantation 21 days post-TIPSS. Another developed a pseudoaneurysm following HA puncture, managed by insertion of a covered stent. One child sustained a bile duct injury and bile leak, which resolved following conservative treatment with antibiotics.
Three children (9%) developed hepatic encephalopathy (HE), which was refractory to medical treatment in 2 cases. In 1 child, the calibre of the TIPSS was reduced to treat post-operative hyperammonaemia and encephalopathy. HE, however, persisted, necessitating another procedure to occlude the TIPSS. In the other child, HE progressed in parallel with an overall deterioration in the child's condition. He became unfit for transplantation and care was withdrawn. Six additional children had asymptomatic post-operative hyperammonaemia.
Six patients developed minor post-operative complications, including pyrexia of unknown origin (n = 2) that was treated with 48 hours of intravenous antibiotics; or nausea and/or localised pain that extended hospital stay by ≥24 hours (n = 4).
Transjugular Intrahepatic Portosystemic Shunt Reintervention to Maintain Patency
Ten children (30%) required intervention to maintain TIPSS patency. The median time to first reintervention was 248 days (range 3 days–2.0 years). Seven children (21%) required >1 intervention. The 1- and 5-year freedom from reintervention was 71% and 55%, respectively (Fig. 3C). Two patients developed early stent occlusion, presenting with recurrent variceal haemorrhage, and requiring urgent stent intervention. Ultrasound screening and surveillance venography identified another 8 patients with TIPSS stenosis who required balloon dilatation.
Variables associated with an increased rate of reintervention were TIPSS diameter; pre-operative ASA score; and indication for TIPSS (symptom control versus bridge-to-transplantation). Multivariate analysis did not identify any variables that independently influenced freedom from reintervention.
The management of paediatric PHTN is primarily focused on the prevention and management of variceal haemorrhage. The role of TIPSS in the current treatment algorithm remains unresolved. This study has reported a series of 40 consecutive patients that underwent attempted TIPSS for resistant, paediatric PHTN. This is the single largest case series published to date, with the longest follow-up.
The procedure was technically successful in 79% of cases and our current success rate is 82%; comparable with results from other paediatric centres (14,15,21). We have also demonstrated that TIPSS can be successful in young infants (20). Although effective, the procedure is, however, technically demanding. Operative and screening times reflect the technical challenges. Despite the use of intra-operative ultrasound in many cases, the median radiation dose for the TIPSS procedure in this series is still equivalent to 2.9 years of background radiation (range 0.5–7 years). This exposure carries a risk of developing a new tumour of 1 in 1900 (range 1 in 800–9900) (22).
PV hypoplasia and abnormal PV configuration were associated with several technical failures within this series. Biliary atresia may be associated with PV hypoplasia (23) but overall was not associated with a greater risk of technical failure in this series. We would recommend that procedural adjuncts be used to help cannulate the PV, especially in patients with PV hypoplasia. Intra-operative ultrasound, wedged hepatic venography, superior mesenteric angiography, and insertion of guidewires and balloons into the PV may all increase technical success rates.
From the available portal pressure data, we have demonstrated that a PSG of <12 mmHg can be achieved in almost 95% of children undergoing TIPSS. This is in keeping with the previous report by Di Giorgio et al (15) and the standards for adult practice (6). This study has confirmed that a successful TIPSS is highly effective at controlling variceal bleeding and refractory ascites in children with resistant PHTN, as previously described (24,25). Furthermore, this study supports the report by Steventon et al that TIPSS may be used to control active haemorrhage and enable children to be listed and undergo successful liver transplantation (19). It may also be used as a bridge-to-transplantation and, in some, may even avoid the need for transplantation in the medium to long-term.
Most TIPSS were uncomplicated. Nevertheless, adverse events did arise within a significant proportion of our study group. HE occurred in 9%. This is less common than that observed in adults (26,27), which may reflect the lower incidence of cirrhosis in paediatric TIPSS candidates. Importantly, HE was more frequent following an emergency TIPSS (25%). This may relate to the large volumes of blood within the gut, which could increase nitrogenous load within the systemic circulation post-TIPSS. Not all HE was responsive to medical therapy.
Inadvertent HA puncture during TIPSS is reported to occur in approximately 6% of adult patients (28). HA injury is, however, much rarer, occurring in 1% of adult cases (23,29) and is previously unreported in a child. Our most serious complication was seen in a child who had previously undergone a size-matched whole-graft liver transplant. HA puncture and catheterisation resulted in extensive hepatic infarction that, in turn, required early re-transplantation. Previous transplantation was not a factor that influenced technical success in this series. Transplantation, especially split liver transplantation, may, however, alter the relationship between the intrahepatic and extrahepatic vasculature, making the procedure more difficult (30–33). It is not clear whether the previous transplant contributed in this case. Nevertheless, we would recommend pre-operative CT angiography to determine the anatomic relationship between the HV and PV in children with previous transplantation.
The clinical status of the child was an important predictor of prognosis, as previously described (33). In this study, Child-Pugh score was the single most important factor in determining long-term outcome post-TIPSS. While more advanced liver disease was associated with worse outcome, this study has also highlighted that TIPSS can be a useful bridge-to-transplantation, even in very ill children.
Finally, 30% of children required reintervention to maintain stent patency within the first year. This is less than that previously reported in paediatric studies (9,11,34) but is substantially higher than that seen in adults (35). This most likely reflects the smaller stent sizes used in paediatric practice. Notably, our earlier use of uncovered stents did not influence the rate of reintervention. We, however, changed our practice in 2000 to use covered endoprosthesis. This coincided with the change in adult practice, where covered stents were introduced to reduce the incidence of in-stent stenosis and shunt occlusion (35–37) and the expectation was that similar benefits would apply to children as well as adults.
The rate of reintervention means that these children should have regular surveillance to identify significant stenosis and enable timely intervention. At our institution, this involves regular ultrasound scans in the first year together with annual TIPSS venography. Children with smaller stent size require particular care. Recurrence of variceal bleeding is a late indicator of stent occlusion and requires urgent investigation and management.
TIPSS is a highly effective management option for children with PHTN resistant to conventional therapy. It may serve as a bridge-to-transplantation or facilitate transplantation in those who would be otherwise unfit due to hemodynamic instability from ongoing bleeding. Advanced liver disease is associated with a comparatively poor long-term outcome post-TIPSS, and clinicians may want to consider alternative treatment options in this group. The procedure is also technically demanding with the risk of causing vascular or biliary injury or precipitating HE. Stent stenosis is common; regular USS and venography should be used to evaluate stent patency and optimise longevity.
The authors gratefully acknowledge the input of Simon Olliff, Queen Elizabeth Hospital, Birmingham, UK, Kamarjit Singh Mangat, National University Hospital, Singapore, and Philip John, The Hospital for Sick Children, Toronto, Canada who performed the majority of the TIPSS procedures.
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