Recanalization of Chronic Portal Vein Occlusion in Pediatric Liver Transplant Patients

CLINICAL STUDY

Recanalization of Chronic Portal Vein Occlusion in Pediatric Liver Transplant Patients Heather Cleveland, BSRS, Sheena Pimpalwar, MD, Daniel Ashton, MD, Alex Chau, MD, Aaditya Nagaraj, MD, and J. Alberto Hernandez, MD ABSTRACT Purpose: To evaluate technical and clinical success and report long-term outcomes of portal vein (PV) recanalization in pediatric orthotopic liver transplant (OLT) patients with chronic PV occlusion. Materials and Methods: This is a retrospective review of 15 OLT patients (5 males) with chronic PV occlusion who underwent PV recanalization (33 procedures) between October 2011 and February 2018. Median age was 4.5 years (range, 1–16 years); median weight was 16.6 kg (range, 11.5–57.3 kg). Median time interval from OLT to first intervention was 3.25 years (range, 0.6–15.7 years). Clinical presentations included hypersplenism (n ¼ 12), gastrointestinal bleeding (n ¼ 9), and ascites (n ¼ 3). One patient had incidental diagnosis of PV occlusion. Primary, primary-assisted, and secondary patency at 3, 6, 12, and 24 months were evaluated. Results: Technically successful PV recanalization and reduction of PV pressure gradient to  5 mm Hg was performed in 13/15 patients (87%). Ten of 15 (67%) patients had successful recanalization with the first attempt. Clinical success, defined as improvement in signs and symptoms of portal hypertension, was achieved in 12/13 (92%) patients. Five of 33 (15%) major complications (Society of Interventional Radiology class C), including perisplenic hematoma (n ¼ 2), hemoperitoneum (n ¼ 2), and hepatic artery pseudo aneurysm (n ¼ 1), were managed with pain medication and blood product replacement. Median follow-up was 22 months (range, 1–77 months). Median primary patency was 5 months. Primary patency at 3, 6, 12, and 24 months was 53.8%, 46.2%, 38.5%, and 30.8%, respectively. Primary-assisted patency was 84.6%, 76.9%, 53.8%, and 46.2%, respectively. Secondary patency was 92.3%, 84.6%, 53.8%, and 46.2%, respectively. Conclusions: PV recanalization is a safe and effective minimally invasive option in the management of chronic PV occlusion after pediatric OLT.

ABBREVIATIONS OLT ¼ orthotopic liver transplant, PV ¼ portal vein

The incidence of post-transplant portal vein (PV) complications in pediatric patients is documented to be as high as 33% (1). PV occlusion accounts for 5.7% of PV complications in pediatric patients (2). PV occlusion is the most

From the Department of Interventional Radiology (H.C., D.A., A.C., J.A.H.), Texas Children’s Hospital, 6621 Fannin Street, Houston, TX, 77030; University of Missouri Health Care (S.P.), Columbia, Missouri; and Baylor College of Medicine (D.A., A.C., A.N.), Houston, Texas. Received May 28, 2018; final revision received August 17, 2018; accepted August 20, 2018. Address correspondence to J.A.H.; E-mail: [email protected] None of the authors have identified a conflict of interest. From the Pediatric Intervention session at the SIR 2018 Annual Scientific Meeting. © SIR, 2018 J Vasc Interv Radiol 2018; ▪:1–7 https://doi.org/10.1016/j.jvir.2018.08.020

common pre-hepatic etiology of portal hypertension after orthotopic liver transplantation (OLT) (3). It can lead to morbidity, graft failure (4–6), and life-threatening variceal bleeding and can make re-transplant difficult (1,4). There are medical, endoscopic, and surgical methods of management of portal hypertension (7); however, angioplasty, with or without stent placement, is emerging as the first treatment option for PV complications (5) due to its minimal invasiveness, low rate of complications, high success rates, and good outcomes (1,8). Endovascular management of PV occlusion is more challenging than PV stenosis. Since reported pediatric studies (4,7,8) present a combination of PV stenosis and occlusion, it is difficult to assess the outcomes of PV occlusion alone from these studies. The aim of this study was to evaluate the technical and clinical success and report the long-term outcomes of PV recanalization in pediatric liver transplant patients with chronic PV occlusion in a single tertiary care center.

2 ▪ Recanalization of Chronic PV Occlusion in Liver Transplant Patients

MATERIALS AND METHODS Patient Characteristics This was a retrospective, institutional review boardapproved pediatric cohort study of 15 OLT patients (5 males; median weight, 16.6 kg, range, 11.5–57.3 kg) with chronic PV occlusion who underwent PV recanalization (33 procedures) between October 2011 and February 2018. During this same period, 217 OLTs were performed on 196 patients at our institution. The electronic medical record was searched for all patients who underwent PV interventions. Patients with PV stenosis were excluded (n ¼ 9). Patient demographics, indication for and type of OLT, and indication for intervention are summarized in Table 1. OLT (age at transplant, 0.4–15.8 years) was performed for biliary atresia (n ¼ 7), biliary atresia with failed Kasai (n ¼ 5), Alagille syndrome (n ¼ 2), and autoimmune hepatitis (n ¼ 1). Only 1 patient underwent transplantation at an outside hospital. Complete PV occlusion with cavernous transformation was diagnosed in all patients by either Doppler ultrasound (n ¼ 6) or magnetic resonance venography (MRV) (n ¼ 9) at a median of 1.9 years (range, 0.6–8.1 years) after OLT. Clinical presentations of portal hypertension included hypersplenism (n ¼ 12), gastrointestinal bleeding (n ¼ 9), and ascites (n ¼ 3). One patient had incidental diagnosis of PV occlusion on ultrasound performed for elevated aspartate aminotransferase/alanine aminotransferase. The time interval between OLT and the first interventional procedure was a median of 3.3 years (range, 0.6–15.7 years).

Technique All procedures were performed under general anesthesia. Pediatric interventional radiologists with adult and pediatric training and 15, 10, 5, and 3 years of experience performed 25, 5, 2, and 1 procedures as the primary operator, respectively. In addition to PV recanalization with angioplasty and stent placement, other procedures, such as roux limb variceal embolization and portosystemic shunt embolization, were performed as needed (Table 2). Pre-procedural mapping of the most favorable access (trans-hepatic, trans-splenic, or both) was done by review of MRV and pre-procedure ultrasound by the primary operator. Ultrasound-guided percutaneous trans-hepatic (n ¼ 15), trans-splenic (n ¼ 13), or combined (n ¼ 5) access using a micropuncture access set (Cook Medical, Bloomington, Indiana) was used to place a 4F x 10-cm vascular sheath (Terumo Medical Corporation, Elkton, Maryland). Pressure measurements of the superior mesenteric and splenic vein were recorded. Intraoperative splenic and/or superior mesenteric venograms were performed using 4F Kumpe (AngioDynamics, Inc, Queensbury, New York) or 4F non-taper angled Glidecath (Terumo Corporation, Shibuya-ku, Tokyo, Japan) (Fig 1) to locate the stump of the occluded PV (“PV

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Table 1. Patient Characteristics (n ¼ 15) Patient characteristics Gender, % female Weight, kg

10 (66.7%) 16.6 (11.5–57.3)

Age at transplant, years*

0.8 (0.4–15.8)

Age at first interventional procedure, years*

3.2 (1–16)

Time interval between transplant and first interventional procedure, years* Indication for transplant

5 (0.6–15.7)

Biliary atresia

7 (46.7%)

Biliary atresia failed Kasai

5 (33.3%)

Alagille syndrome

2 (13.3%)

Autoimmune hepatitis

1 (6.7%)

Transplant type Whole-liver OLT Split-liver OLT

10 (66.7%) 5 (33.3%)

OLT ¼ orthotopic liver transplant *Values are median (range).

stump”). Once located, a combination of products, such as a 0.035”-angled Glidewire (Terumo), a 0.035’’ Roadrunner (Cook), a 0.018”-angled Glidewire (Terumo), an angled or straight CXI catheter (Cook), or a 0.035” or 0.018” Quick-Cross catheter (Spectranetics Corporation, Colorado Springs, Colorado), were used to probe the PV stump. Whenever PV recanalization was unsuccessful using the trans-hepatic approach, further attempts were made using a combined transhepatic/trans-splenic approach (n ¼ 5) during the same procedure and vice versa. All patients were positioned to allow biplane fluoroscopy. When visualizing/crossing the PV occlusion on single-plane fluoroscopy (n ¼ 8) was difficult, the lateral plane was additionally used. Similarly, cone-beam computed tomography (n ¼ 4) was used in difficult cases to assist with finding the best working angle for visualization and crossing of PV occlusion. Once the PV occlusion was crossed and confirmed by portal venography, intrahepatic PV pressure was measured, and the pressure gradient across the occluded PV was calculated (median, 8 mm Hg; range, 2–15 mm Hg). An intravenous heparin bolus (50–75 IU/kg) was administered. The initial crossing wire was exchanged for a 0.035’’ Amplatz Super Stiff guidewire (Boston Scientific, Global Park, Heredia, Costa Rica) that was used as the working wire for serial angioplasty using 6–12 mm x 4 cm Mustang (Boston Scientific, Galway, Ireland) or Conquest (Bard Peripheral Vascular Inc, Tempe, Arizona) balloons (Table 2). Balloons were inflated between nominal and rated burst pressure for 1–2 minutes, resulting in reduction of PV pressure gradient to a median of 1 mm Hg (range, 0–5 mm Hg). PV stent (n ¼ 4) was placed only if there was residual venous pressure gradient despite successful angioplasty and for recurrence of PV stenosis/ occlusion during follow-up. The vascular access sheath was upsized (n ¼ 17) as needed during these interventions.

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Table 2. Interventional Procedure Details (n ¼ 33) Patient 1

Procedures Performed fPVR, RLE fPVR, RLE PV stent PVR, PSE

2

Approach

Balloon Sizes Used (mm)

TS TS TS TH

3, 6, 7 6, 8

TS TH TH, TS

3, 5, 6, 7 6, 8 6

Stent Used

8 mm x 4 cm E-Luminexx

Complication (SIR class)

Follow-up (months)

C

28

B A

6

B

46

3

PVR PVA PV stent, PSE

4

PVR dPV

TH TH

5, 8

5

PVR PVA

TH TH

6, 8 8, 9

6

PVR PVA PVA

TH, TS TH TH

6, 8 10 10, 12

C B

25

7

PVR PVA, RLE

TS TS

4, 6, 8 8, 9

C

9

8

PVR, RLE

TH

8, 10

B

7

9

fPVR PVR, RLE PVR PV stent

TH, TS TH, TS TH TH

C B

9

fPVR, RLE PVR dPV

TH,TS TH TH

10

11 12

PVR PV stent PVR dPV

6, 8 8, 9 6

TH

fPVR, RLE fPVR, RLE fPVR, RLE

TH TS TS

15

fPVR

TS

8 mm x 27 mm Express LD, 6 mm x 17 mm Express LD

B 4

8, 10

PVR, PSE

22

5, 6, 8, 10, 12 6, 8, 10 6, 8, 10 10

14

42 B

TS TS TS TS

13

8 mm x 3 cm E-Luminexx

A 64 8mm Palmaz A

77

C

1

dPV ¼ diagnostic portovenogram; fPVR ¼ failed portal vein recanalization; PSE ¼ portosystemic shunt embolization; PV ¼ portal vein; PVA ¼ portal vein angioplasty; PVR ¼ portal vein recanalization; RLE ¼ roux limb variceal embolization; TH ¼ trans-hepatic; TS ¼ transsplenic

Lastly, tract embolization using Gelfoam pledgets (n ¼ 25) (Pharmacia & Upjohn Company, Kalamazoo, Michigan) or microfibrillar collagen hemostat (n ¼ 7) (Davol, Inc, Warwick, Rhode Island) was performed through the vascular access sheath (4F–8F) under ultrasound guidance. Postprocedure anticoagulation (n ¼ 23) was performed in consultation with the hematology service. Complications were classified according to the Society of Interventional Radiology (SIR) (9).

Follow-up Patients were followed-up by the institutional liver transplant service and the interventional radiology clinic. A baseline postoperative ultrasound on the first post-procedure day was performed in all patients. In the earlier part of the study, further imaging (ultrasound or MRV) was performed

only if clinically indicated. During the latter part of the study, a post-procedure imaging protocol was followed constituting ultrasound Doppler at 1, 3, 6, and 12 months and yearly thereafter. Post-procedure platelet counts were compared with pre-procedure values.

Definitions Technical success was defined as successful PV recanalization and reduction of portal venous pressure gradient to  5 mm Hg. Clinical success was defined as improvement in all presenting signs and symptoms of portal hypertension, such as ascites, variceal bleeding, and thrombocytopenia. Primary, primary-assisted, and secondary patency were reported according to Society of Vascular Surgery reporting standards (10). Primary patency was defined as the time from primary intervention to first imaging diagnosis of

4 ▪ Recanalization of Chronic PV Occlusion in Liver Transplant Patients

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Figure 1. A 4-year old female with a history of biliary atresia presented with gastrointestinal bleeding 39 months after whole-liver OLT. She was diagnosed with PV occlusion with cavernous transformation on MRV imaging 20 months before the procedure. (a) Contrastenhanced MRV with multi-planar reformation demonstrating the “PV stump” (arrow), splenic vein (open star), and superior mesenteric vein (SMV) (arrow head). (b) Venogram via 4F non-taper angled Glidecath from trans-splenic approach demonstrating PV stump (arrow), splenic vein (open star), and SMV (arrow head). (c) Hand injection at the PV stump (arrow), demonstrating collaterals (open star) to the intrahepatic portal vein (arrow head) with splenic vein pressure of 25 mm Hg. (d) Post-angioplasty venogram demonstrating patent recanalized PV (arrow head) from the stump (arrow), 4F non-taper angled Glidecath (Terumo) in the splenic vein from trans-splenic approach, and Aurous centimeter sizing catheter (Cook) across the PV and seated in the SMV from the trans-hepatic approach with a 4-mm Hg PV pressure gradient. (e) Venogram performed 2 months after recanalization from trans-hepatic approach via 4F Soft-Vu pigtail catheter (AngioDynamics) placed in the SMV, demonstrating recurrent stenosis (arrow head) with 8 mm Hg PV pressure gradient (f) Post-recurrent PV stenosis (arrow head) venogram resulting in 1-mm Hg PV pressure gradient from transhepatic approach via 4F Soft-Vu pigtail catheter (AngioDynamics) placed in the SMV. (g) Ultrasound follow-up 12 months after angioplasty, demonstrating patent PV (arrow head).

either PV restenosis or PV thrombosis (7). Primary-assisted patency was defined as the time from primary intervention to first imaging diagnosis of PV restenosis requiring

intervention. Secondary patency was defined as the time from primary intervention to first imaging diagnosis of PV thrombosis requiring intervention.

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Table 3. Patency Rates of PV Recanalization (n ¼ 13) 3 months % (n)

6 months % (n)

12 months % (n)

24 months % (n)

36 months % (n)

60 months % (n)

Primary patency

53.8 (7)

46.2 (6)

38.5 (5)

30.8 (4)

15.4 (2)

7.7 (1)

Primary-assisted patency

84.6 (11)

76.9 (10)

53.8 (7)

46.2 (6)

30.8 (4)

15.4 (2)

Secondary patency

92.3 (12)

84.6 (11)

53.8 (7)

46.2 (6)

30.8 (4)

15.4 (2)

PV ¼ portal vein.

RESULTS Technical Success

76.9%, 53.8%, and 46.2%, respectively. Secondary patency at 3, 6, 12, and 24 months was 92.3%, 84.6%, 53.8%, and 46.2%, respectively.

A total of 33 procedures were performed on 15 patients. Technically successful PV recanalization was performed in 13/15 patients (87%). Ten of 15 (67%) patients had successful recanalization during the first attempt/procedure; 2/15 patients had successful recanalization during the second procedure; and 1/15 patients had successful recanalization during the third procedure. PV stent was placed in 4 patients as follows: (1) Patient 1—8 mm x 40mm Luminexx (Bard) for residual pressure gradient; (2) Patient 11—Palmaz (Cordis) dilated to 8 mm during the second procedure for recurrent stenosis; (3) Patient 3—8 mm x 30 mm Luminexx (Bard) during the third procedure for recurrent stenosis; and (4) Patient 9—combination of 8 mm x 27 mm and 6 mm x 17 mm Express LD (Boston Scientific) stents during the fourth procedure for recurrent occlusion. The median procedure time was 3.6 hours (range, 1.4–9.9 hours), and the median radiation dose was 303.2 mGy (range, 16.8–7933 mGy). Post-procedure anticoagulation was operator dependent, which included no anticoagulation in 10/33 (30%) patients; heparin (18 U/kg/hour x 24 hours) transitioned to therapeutic lovenox in 14/33 (42%) patients; therapeutic lovenox only in 8/33 (24%) patients; and baby aspirin in 1/33 (3%) patients.

A total of 10/33 (30%) minor complications occurred. Postprocedure abdominal pain that resolved spontaneously (n ¼ 1), hematuria from urethral trauma caused by Foley catheter placement that resolved in 1 day (n ¼ 1), and clot in the lower pole of the spleen after trans-splenic access that resolved without any intervention (n ¼ 1) were classified as SIR class A. Post-procedure abdominal pain (lasting less than 48 hours) treated with medication (n ¼ 7), 3 of which also had a fever > 100  F for less than 24 hours, were classified as SIR class B. Five of 33 (15%) major complications (SIR class C) occurred. These included perisplenic hematoma (n ¼ 2) treated with pain medication; hemoperitoneum (n ¼ 2) treated with pain medication, blood transfusion, and observation in the intensive care unit; and hepatic artery pseudo aneurysm (n ¼ 1) in the trans-hepatic access tract managed with pain medication, discontinuation of anticoagulation, and manual pressure. Trans-splenic approach was used in 4/5 procedures with major complications (4/13, 31%) and in both patients with hemoperitoneum.

Clinical Success

DISCUSSION

Clinical success was achieved in 12/13 (92%) patients. All 8 patients who presented with gastrointestinal bleeding and 3 patients with ascites had complete resolution of their presenting symptoms. Eleven of 12 patients with pre-procedure thrombocytopenia (median, 88 platelets/mcL; range, 32–118 platelets/mcL) responded with a median increased platelet count of 52.1% (median, 169 platelets/mcL; range, 150–282 platelets/mcL). The only clinical failure in this study was a patient with pre-procedure thrombocytopenia. Despite technical successful PV recanalization and resolution of gastrointestinal bleeding, this patient did not demonstrate an increase in platelet count.

PV Patency At a median follow-up of 22 months (range, 1–77 months), median primary patency of the recanalized PV was 5 months (Table 3). Primary patency at 3, 6, 12, and 24 months was 53.8%, 46.2%, 38.5%, and 30.8%, respectively. Primaryassisted patency at 3, 6, 12, and 24 months was 84.6%,

Complications

PV recanalization and angioplasty with or without stent placement has proven to be an advantageous treatment option for post-transplant PV stenosis and occlusion because it not only re-establishes hepatopedal flow but also treats hypersplenism secondary to portal hypertension (11). Several reports have described successful pediatric PV recanalization, affirming this procedure as a feasible alternative to conventional surgical revisions (4,5,7,12–18). A unique aspect of the present study was the use of the transsplenic approach in addition to the trans-hepatic approach as a primary approach for PV recanalization based on review of pre-procedural imaging. Visualization of a conical PV stump was considered a favorable target, and trans-splenic approach was selected when the apex of this stump pointed toward the liver. In 1 case, crossing the PV occlusion with 1 approach and snaring the crossing wire with the second approach was also used (n ¼ 1). Thus, trans-hepatic (15/33) and trans-splenic (13/33) approaches were used in nearly equal numbers in the current study to facilitate

6 ▪ Recanalization of Chronic PV Occlusion in Liver Transplant Patients

technical success. Similar to the present study, Uller et al (8) used trans-splenic access in 3/8 patients and described the following advantages of this approach: (1) ability to obtain orthograde portography and optimal lesion characterization in young children with small portal branches; (2) useful approach for recanalization of PV occlusion; and (3) useful approach for traversing angled stenotic portal vein segments. In comparison, most reported studies used only the trans-splenic approach after failure of the trans-hepatic approach (7,17). Most pediatric studies in the literature report technical success on a combined group of patients with either PV stenosis or occlusion, making a comparison with the present study difficult. The technical success of the present study (87%) was similar to that reported by Ko et al (14) for PV stent placement in 10/12 (83%) children but inferior to 2 other pediatric studies—Patel et al (7) (98%) and Yabuta et al (4) (98%)—comprising a majority of PV stenosis. Key elements that contributed to the technical success of PV recanalization in this study were 1) review of pre-procedure imaging, which allowed for a full picture of the transplant anatomy and more precise location to probe with the wire at the PV stump; 2) the use of combined access techniques when necessary; 3) the use of supportive sheaths as well as various catheter and wire combinations to improve support and torquability of the catheter and wire; and 4) persistence—do not give up too soon. These can be long procedures with beneficial outcomes. The clinical success (92%) of the present study was, however, superior to previous pediatric reports by Ko et al (14) (83%), Yabuta et al (4) (86%), and Patel et al (7) (90%). The primary patency (median, 5 months) and longterm patency rates are inferior to those previously reported (4). This may be related to the shorter duration of follow-up and the fact that the current study was focused only on patients with PV occlusion, whereas previous reports had more representation of PV stenosis. Stent placement should be used restrictively in the pediatric liver transplant population for potential complications, such as PV thrombosis, in-stent or stent edge restenosis, functional stent stenosis in the growing child, stent deformity and fracture during follow-up, and difficult reanastomosis if repeat liver transplantation is necessary (7,8,14,16). In the literature, criteria used as indication for stent placement are suboptimal angioplasty result with residual pressure gradient >5 mm Hg or elastic recoil of more than 50%; recurrence of PV stenosis within 3–6 months (6); and management of PV kinking (8,14). In keeping with a conservative approach for stent placement in children, and similar to other pediatric studies (7,8,14), only 4/13 patients required stent placement for residual pressure gradient, recurrent stenosis, or recurrent occlusion, all of whom had no recurrence of clinical symptoms and patent PV at the end of the study period. In PV interventions, minor complications such as postprocedural abdominal pain and fever are common and can be managed with medications (19). Hemoperitoneum is the most feared major complication of percutaneous trans-

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hepatic as well as trans-splenic (19) portal venous angioplasty and stenting (1). In a study of 44 children, Pimpalwar et al reported a 27% bleeding complication rate with transsplenic access. Of the risk factors studied, the authors found that periprocedural anticoagulation had a statistically significant co-relation with the risk of intraperitoneal bleeding. In the current study, both patients with hemoperitoneum had trans-splenic access, 1 of whom received periprocedural anticoagulation. The trans-splenic approach is valuable but is not used without the known feared bleeding risk (19), which was 15% (2/13) in the present study and lower than in the Pimpalwar et al (19) study. The technical and clinical success of endovascular treatment of PV stenosis and occlusion have recently opened the gateway to offering this management to asymptomatic patients. Yabuta et al (4) included asymptomatic patients in their retrospective study of 43 patients diagnosed using ultrasound Doppler. Gao et al (20) also recommended early diagnosis of PV stenosis using Doppler ultrasound and computed tomography and treatment of PV stenosis with a pressure gradient of 5 mm Hg irrespective of the appearance of clinical symptoms. Only 1 patient in the present study had incidental diagnosis of PV occlusion that was successfully treated. Postoperatively, this patient demonstrated resolution of ascites and increased platelet count. Further prospective studies would be helpful to study whether this approach could decrease the risk of graft failure and portal and pulmonary hypertension This study was limited by its small sample size and retrospective nature. Because the sample size was small, statistical analysis would be misleading. While a prospective study would be ideal, it is limited by the small unique population in a tertiary care pediatric center and would require multicenter cooperation. In conclusion, PV recanalization is a minimally invasive procedure with excellent technical and clinical success for management of post-transplant chronic PV occlusion in children.

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