Endovascular treatment of acute and chronic portal vein thrombosis in patients with cirrhotic and non-cirrhotic liver

Abstract

Background

Treatment of patients with portal vein thrombosis (PVT) differs due to different etiology and wide range of symptoms but certain patients seems to benefit from endovascular intervention.

Purpose

To assess the safety and efficiency of endovascular treatment of acute and chronic PVT in patients with cirrhotic and non-cirrhotic liver.

Material and Methods

Twenty-one patients with PVT treated with an endovascular procedure in 2002–2013 were studied retrospectively. Data on etiology, onset and extension of thrombus, presenting symptoms, methods of intervention, portal pressure gradients, complications, recurrence of symptoms, re-interventions, clinical status at latest follow-up, and survival were collected.

Results

Four non-cirrhotic patients with acute extensive PVT and bowel ischemia were treated with local thrombolysis, in three combined with placement of a transjugular intrahepatic portosystemic shunt (TIPS) placement. Three recovered and have survived more than 6 years. In six non-cirrhotic patients with chronic PVT and acute or threatening variceal bleeding recanalization and TIPS were successful in three and failed in three. Eleven cirrhotic patients with PVT and variceal bleeding or refractory ascites were successfully treated with recanalization and TIPS. Re-intervention was performed in five of these patients and five patients died, three within 12 months of intervention. Four cirrhotic patients had episodes of shunt-related encephalopathy and three had variceal re-bleeding.

Conclusion

TIPS was found to be effective in reducing portal hypertension in patients with PVT. In patients with extensive PVT and bowel ischemia treatment with TIPS combined with thrombolysis should be considered.

Keywords

Portal vein thrombosis liver cirrhosis endovascular procedure retrospective study

Introduction

There is no general consensus regarding treatment of patients with portal vein thrombosis (PVT) (1). The most common cause of PVT is liver cirrhosis, the occurrence of which increases with progressive disease. Non-cirrhotic PVT can be secondary to thrombogenic disorders, infections, malignancies, and inflammatory diseases (2). The prevalence of PVT in cirrhotic patients is 10–25% (3). The prevalence in the non-cirrhotic population is unknown but PVT is estimated to cause 5–10% of all cases of portal hypertension in the Western hemisphere (4).

PVT leads to portal hypertension, i.e. an increased difference in pressure between the portal and hepatic veins. In cirrhotic patients gastroesophageal varices develop at a gradient of 10–12 mmHg and at gradient >12 mmHg there is high risk of variceal bleeding (5), associated with a 6-week mortality rate of 10–20% (6). Other possible consequences of portal hypertension are ascites, hydrothorax, hepatorenal syndrome, and hypersplenism. Spontaneous recanalization of PVT is rare. With systemic anticoagulation treatment partial or complete recanalization can be achieved at rates of 33–75% (7 –9). PVT can progress during anticoagulation and does so in more than one-fourth of patients after stopping anticoagulation (7). Extension of PVT into the superior mesenteric vein (SMV) is associated with poor outcome due to the risk of bowel ischemia (10). PVT was previously considered a relative contraindication for treatment with transjugular intrahepatic portosystemic shunts (TIPS), but TIPS are now being used with promising results in these patients (9,11 –14). Treatment with local thrombolysis is an option in patients with acute PVT and bowel ischemia, and even though complication rates are high and recanalization rates low most reports claim an improvement in symptoms after intervention (15 –17).

The aim of this study was to report the results of endovascular treatment of PVT at our hospital.

Material and Methods

A retrospective review of the log of endovascular interventions during 2002–2013 at our hospital identified a total of 21 patients (15 men, 6 women; mean age, 53 years; age range, 20–75 years), with PVT treated with endovascular procedures. Clinical data, including onset of symptoms and estimated age of thrombosis at intervention, were collected from our medical records and the referring hospitals. In patients with cirrhosis, liver function was assessed using the Child-Pugh score (18).

PVT was diagnosed using computed tomography (CT) performed with contrast enhancement in the venous-portal phase. Acute PVT was defined by the absence of collaterals and the rapid onset of abdominal pain, intestinal ischemia, and/or infarction within 14 days of the diagnosis. Chronic PVT was defined as a decrease in intra-luminal density in the portal vein, a replacement of the original main portal vein (MPV) with a fibrotic cord, or a portal cavernoma.

The patients were selected for endovascular intervention because of an insufficient response to conservative treatment. Bowel ischemia with portal vein (PV) and SMV thrombus was the indication for endovascular intervention of acute PVT in four patients, abdominal pain but without SMV involvement in one, and recurrent severe variceal bleeding in another patient. The indication for endovascular intervention in patients with chronic PVT was acute/high risk of variceal bleeding in 14 and refractory ascites in one. Patients with very large varicose veins combined with previous episodes of gastro-intestinal bleeding, thrombocytopenia, and/or in need of surgery were considered to have a high risk of variceal bleeding. Patients with variceal bleeding were treated with current standard methods, such as band ligation, vasoactive drugs, and antibiotics prior to endovascular treatment.

The aim of intervention was to reduce portal hypertension by creation of a TIPS and/or recanalization of the portal vein. Informed consent was obtained, and retrospective study of logs and charts was approved by the ethical committee 2012-11-07 (Dnr2012/134).

Endovascular methods

Portal venography was done after ultrasound-guided transhepatic puncture of a right-sided branch of the PV through a 1.33-mm catheter placed proximally in the MPV or SMV. After recanalization, the thrombus and/or stenosis was dilated with 8–10 mm balloons and when needed, bare metal stents were used to keep the lumen patent.

TIPS was performed according to standard methods as previously described (12), with guidance of a wire through the portal venography catheter positioned in the PV branch chosen for target site. The gradient between the pressure of the right atrium and the PV was used to estimate the gradient between the hepatic veins and the PV, in occlusive PVT the gradient was not always obtainable. Covered stents were used in all patients, except in one who had an uncovered stent, and were dilated to 8mm. Embolization of collaterals, when performed, was achieved using coils.

Transhepatic thrombolysis: Portal venography and recanalization were performed as described above except for the one patient who had a TIPS followed by thrombolysis through the sheath in the same session. In two patients, mechanical thrombectomy catheters were used: Rotarex in one patient and Aspirex in the other (Straub Medical, Wangs, Switzerland). An infusion catheter was placed through the thrombi, with the distal end in the free lumen of the MPV or SMV. A bolus dose of 2–8 mg of Actilyse® (Boehringer Ingelheim, Ingelheim am Rhein, Germany) was injected followed by infusion of 1–2 mg per hour until the next venography was performed. Thrombolysis was discontinued when no further recanalization was achieved or if major hemorrhage occurred.

Embolization of the transhepatic puncture canal with embolization coils ended the procedures. Then antibiotics (cefotaxim) was administered intravenously before intervention.

The degree of recanalization was evaluated with venography after intervention and considered: (i) complete, if no intravascular material remained and blood flow was restored; (ii) partial, if the thrombosis was less extensive after intervention than before; or (iii) unchanged. Only major complications were reported, defined as those that required any type of intervention, therapy, or prolonged hospitalization. Endpoints were the latest follow-up (range, 1.5 months to 6 years; median, 17 months), death, or liver transplantation.

Results

PVT onset, extension, interventions, patency, and clinical outcome for each patient are presented in Table 1 (online only). Eleven patients had liver cirrhosis, which was considered the main cause of the PVT: one of them also had a thrombogenic disorder. In 10 non-cirrhotic patients, the underlying cause of the PVT was thrombogenic (polycythemia vera, essential thrombocytosis, thalassemia minor, Waldenström's macroglobulinemia, hypercoagulability of unknown etiology, and idiopathic thrombocytopenia) in seven, unknown in one, post-inflammatory in one, and post-surgical in one. None of the patients had malignant PVT. The onset of PVT was acute in six patients and chronic in 15 patients. In 15 patients the thrombus was occlusive, in six patients the thrombus filled >50% of the lumen of the involved vessels, and seven patients had extensive thrombosis with involvement of at least the SMV. The frequency of extensive PVT was higher in patients with a history of thrombogenic disease (4/7) than in patients with cirrhosis (3/11).

Table 1.

Medical history, classification of thrombus, endovascular interventions, complications, and post-interventional status of each of the 21 patients in the study group.

Patient no.	Cirrhosis	Onset	Indication	SMV involvement	Intervention	Complications	Re-intervention	TIPS and recanalization patency	Re- bleeding	Clinical status at endpoint
1	No	A	Intestinal ischemia	Yes	TIPS and thrombolysis	Hematoma, sepsis	No	Occlusion	No	Dead
2	No	A	Intestinal ischemia	Yes	Transhepatic thrombolysis	Infection	TIPS and thrombolysis TIPS dilatation	Patent	No	No recurrent symptoms
3	No	A	Intestinal ischemia	Yes	Transhepatic thrombolysis	Hemothorax	No	Occlusion	No	No recurrent symptoms
4	No	A	Intestinal ischemia	Yes	Transhepatic thrombolysis	Hematoma × 2	Coiling hepatic artery TIPS and thrombolysis Coiling hepatic artery	Occlusion	No	No recurrent symptoms
5	No	C	Large varices. previous bleeding	No	TIPS	Encephalopathy	TIPS dilatation	Patent	Yes	No recurrent symptoms
6	No	C	Acute variceal bleeding	No	Portal venography	No	Not applicable	Not applicable	No	No recurrent symptoms
7	No	C	Large varices pre surgery	No	TIPS		No	Patent	No	No recurrent symptoms
8	No	C	Large varices and previous bleeding	No	Portal venography	No	Not applicable	Not applicable	No	No recurrent symptoms
9	No	C	Large varices, thrombocytopenia	No	Recanalization Portal PTA and stent	No	Recanalization	Occlusion	No	No recurrent symptoms
10	No	C	Previous variceal bleeding	No	Recanalization TIPS	No	No	Patent	No	No recurrent symptoms
11	Yes	A	Large varices, thrombocytopenia	No	Recanalization TIPS	Encephalopathy	No	Patent	No	Liver transplant
12	Yes	A	Acute variceal bleeding	No	Recanalization TIPS	–	No	Patent	No	No recurrent symptoms
13	Yes	C	Acute variceal bleeding	No	Recanalization TIPS	Occult hematoma	No	Patent	No	Dead
14	Yes	C	Acute variceal bleeding	Yes	Recanalization Portal PTA	No	TIPS	Occlusion	No	No recurrent symptoms
15	Yes	C	Refractory ascites	Yes	Recanalization TIPS	Sepsis, encephalopathy	No	Occlusion	No	Dead
16	Yes	C	Acute variceal bleeding	No	Recanalization TIPS and portal stent	Puncture site infection, encephalopathy	Thrombolysis, thrombolysis and TIPS dilatation	Occlusion	No	Dead
17	Yes	C	Acute variceal bleeding	No	Recanalization TIPS and portal stent	Encephalopathy	No	Patent	Yes	Dead
18	Yes	C	Acute variceal bleeding	No	Recanalization TIPS	Hematoma from liver puncture site	Embolization of collaterals	Patent	No	Dead
19	Yes	C	Acute variceal bleeding GAVE	Yes	Recanalization TIPS Portal stent	Pulmonary embolism	Recanalization TIPS dilatation, embolization of collaterals	Patent	Yes	No recurrent symptoms
20	Yes	C	Acute variceal bleeding	No	Recanalization TIPS transplenic	No	Recanalization	Patent	Yes	No recurrent symptoms
21	Yes	C	Large varices previous liver transplant	No	Recanalization TIPS Portal stent	No	No	Patent	No	Liver transplant

A, acute; C, chronic; SMV, superior mesenteric vein.

The use of medical anticoagulation therapy varied due to different symptomatology, thrombophilic states and referring hospitals. Variceal bleeding and thrombocytopenia were the main reasons for no anticoagulation. Six patients were anticoagulated before intervention; in one treatment was discontinued due to gastrointestinal bleeding after intervention; the rest had continued treatment. Eight patients started anticoagulation therapy after intervention and seven patients had no anticoagulation at all.

Four non-cirrhotic patients presented with symptoms of bowel ischemia, and CT demonstrated extensive acute PVT and swollen bowels. All were treated with local thrombolysis, three transhepatically and one transjugularly through a TIPS, with partial recanalization in all four. Renewed thrombolysis combined with TIPS was undertaken in two of these patients 2–3 weeks later due to occlusion, but both re-occluded within 24 h. After successful dilatation, the TIPS remained patent in one of them (Fig. 1). Three of the patients had hemorrhage from the liver puncture, which required premature discontinuation of thrombolysis. All required blood transfusions and one patient also had embolization of hepatic arteries. Two patients had blood-culture confirmed septicemia. One patient developed a short stenosis of the jejunum that was treated surgically, but none of the patients needed extensive bowel resection. Three of the patients recovered and were free of symptoms at latest follow-up. The patient with thrombolysis through the TIPS died 6 weeks after intervention due to progressive liver failure.

Fig. 1.

Non-cirrhotic patient with essential thrombocytosis who presented with abdominal pain. CT (a) showed thrombosis in the main portal vein (MPV) (white arrow) and the superior mesenteric vein, edematous small bowel (black arrow) and ascites (white arrowheads). Portal venogram (b) after partial recanalization of the MPV (white arrow) with local thrombolysis. Venogram (c) after recanalization and TIPS insertion and a later dilatation of the stent showed that good blood flow through the shunt (arrow) was accomplished.

Six non-cirrhotic patients presented with acute/threatening variceal bleeding and chronic PVT. In three of them, recanalization of the MPV and TIPS was successful. The gradient between the portal and the hepatic veins was reduced from 17 mmHg (range, 15–22 mmHg) to 4 mmHg (range, 3–5 mmHg) and the TIPS stayed patent, in one patient after re-dilatation (Fig. 2). One of the patients had an episode of variceal re-bleeding, and one patient had episodes of encephalopathy. In another patient complete recanalization of the MPV was achieved with PTA and a stent but recanalization could not be obtained after re-occlusion. In two patients, scheduled for TIPS, recanalization failed but both were free of symptoms at follow-up. None of the patients had any procedure-related complications and there were no deaths in this group.

Fig. 2.

Non-cirrhotic patient with Waldenström's macroglobulinemia, chronic PVT and recurrent variceal bleeding. CT (a) showed cavernous transformation of the main portal vein (MPV) (white arrow) and classic signs of portal hypertension with large collateral veins (black arrow), ascites (white arrowheads), diffuse mesenteric stranding and splenomegaly (*). Portal venogram (b) confirmed the finding of a cavernous MPV (white arrow). Venogram (c) after partial recanalization and an established connection between liver vein and the portal vein showed reversed blood flow into large collaterals (black arrow). Venogram (d) after stent insertion showed good flow through the TIPS (blank arrow) and reduced flow into collateral veins (black arrow).

Eleven cirrhotic patients presented with acute/threatening variceal bleeding (10 patients) or refractory ascites (one patient). Two patients had acute PVT and nine had chronic PVT, three with extension into the SMV. Recanalization of the MPV and primarily successful TIPS were performed in all. The gradient between the portal vein and the hepatic veins was reduced from 17 mmHg (range, 11–23 mmHg) to 5 mmHg (range, 1–6 mmHg) in the seven patients in whom the gradient was obtained. Complications were hematomas in two, pulmonary embolism in one, septicemia in one, infection at liver puncture site in one, and post-TIPS encephalopathy in four patients. Three patients had variceal re-bleeding: one due to TIPS occlusion, successfully treated with recanalization; one patient due to progressive liver failure (this patient died 16 months after TIPS), and in one patient due to gastric antral vascular ectasia (GAVE). Five of the eleven patients had TIPS occlusion and two of them died after 2 and 4 months, respectively. Five patients had re-interventions: one had a TIPS after re-occlusion of primary MPV recanalization; one had TIPS occlusion twice (treated with recanalization and thrombolysis); one had embolization of collaterals; one had TIPS recanalization; and one patient had recanalization and dilatation of the TIPS twice followed by embolization of collaterals. In eight patients the TIPS was patent at 12-month follow-up or until death. Two patients with patent shunts had a liver transplant. Three of the patients with a patent shunt died after 2.5, 16, and 40 months, respectively. All five deaths in this group of patients were due to progressive liver failure. All 11 patients had Child-Pugh class B at presentation and there was no significant change after TIPS insertion.

Discussion

The choice of treatment of PVT depends on the presenting symptoms but is difficult because some patients are asymptomatic, while others develop life-threatening complications. The result of treatment of PVT is equally difficult to evaluate because outcome depends not only on presenting symptoms but also on extension of the thrombus and whether it is acute or chronic, partial or occlusive. Our classification of acute PVT was similar to that suggested by Han (19), which combines the time aspect with symptoms and radiological findings. However, it is impossible to be sure of whether the PVT was truly acute or not because chronic PVT may be silent at first and become symptomatic due to extension of the thrombus. Treatment strategies vary from none to medical anticoagulation, endovascular intervention with recanalization with PTA, stents, TIPS and thrombolysis, and surgical treatment. The risk of severe complications with more aggressive techniques has to be balanced with the risk of the disease itself, with its complications such as variceal bleeding, ascites, and intestinal ischemia.

This paper focused on our experience with different interventional techniques in patients divided into three groups based on onset and presence of liver cirrhosis. The patients with acute PVT and non-cirrhotic liver were aggressively treated with local thrombolysis, three of them in combination with TIPS, as the goal of treatment of acute PVT was to reconstruct the blocked veins. Only partial recanalization was achieved and re-occlusion took place in an early stage. However, premature discontinuation of thrombolysis due to hematomas can have affected the grade of recanalization and delayed post-interventional anticoagulation treatment. We cannot conclude whether the aggressive treatment had any impact on disease progress, but three patients recovered clinically and are alive more than 6 years after intervention. One death in four patients and no extensive bowel resection is acceptable as reported mortality in bowel infarction is as high as 50% (20). The difficulty of treating patients with extensive acute PVT is clearly reflected in the literature, and the latest consensus meeting stated that there is insufficient evidence in favor of interventional treatment and that systemic anticoagulation should be the treatment of choice (6). However, there are a number of small studies favoring local thrombolysis in selected patients (21,22), in spite of the high frequency of major complications (15). To avoid bleeding from the liver capsule, thrombolysis should be performed transjugularly through the TIPS, even though the procedure is technically more difficult without use of a portal guide. Carbon-dioxide-wedged hepatic venography (23) and balloon occlusion hepatic venography (24) are other methods to visualize the intrahepatic PV, if persistent, and can be considered for guidance.

In chronic PVT, an extensive thrombus is a negative predictor for complete recanalization and long-term prognosis (14), and due to fibrotic transformation of vessels it is hard to completely differentiate vessels from thrombogenic tissue. In this study, the main aim was the decompression of varices with the use of endovascular shunts, and this was achieved with great technical success, even though we included patients with acute variceal bleeding in whom high procedure-related mortality has been reported (25). In the 15 patients in whom a shunt was attempted, the procedure failed in only two, both non-cirrhotic patients with extensive chronic PVT. This supports earlier studies that TIPS can be a safe method for decompression of varices in both cirrhotic and non-cirrhotic patients (11,26).

The rate of TIPS dysfunction in cirrhotic patients was 45%, which is higher than reported in patients without PVT (27). The reason for this might be the long recanalization tract. Encephalopathy occurred at about the same rate as in previous studies (9,14,19), and all patients with a measured gradient after TIPS who developed encephalopathy had a gradient of 5 mmHg or lower, which has been shown to increase the risk (28). Patients with a history of encephalopathy should be carefully evaluated before intervention because TIPS may cause exacerbation (29). Even though the study included one patient with GAVE, which is known to be unresponsive to reduction of portal pressure (30), the rate of re-bleeding was very low.

The cirrhotic group had the highest mortality with survival rates of 100%, 73%, and 55% at 1, 12, and 24 months, respectively, which are in accordance with previous studies (4) and better than the 12-month survival rate of 53% reported in a national multicenter study with less interventional treatment (2). Cirrhotic patients with PVT have a higher mortality than those without PVT (31), but with recanalization and TIPS, survival rates can be as high as 96% and 79% at 12 and 24 months, respectively (32), suggesting that endovascular treatment may improve survival.

The biggest limitations of the study were that the study group was small and heterogeneous and that patients were referred from different parts of the country. It is impossible to know whether there were patients with PVT similar symptoms who were not referred to our center, and the clinical outcome of the total number of patients with PVT in our area during the time period of study is thus unknown.

In conclusion, the results suggest that in patients with PVT and threatening symptoms of portal hypertension, endovascular recanalization and TIPS should be considered. Even in challenging cases with PVT, TIPS can be accomplished in a safe and effective way to decompress portal hypertension, which reduces the risk of life-threatening complications like variceal bleeding and bowel ischemia.

Footnotes

Conflict of interest

None declared.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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