Cardiovasc Intervent Radiol DOI 10.1007/s00270-015-1058-7

CLINICAL INVESTIGATION

Hepatic Tract Plug-Embolisation After Biliary Stenting. Is It Worthwhile? Adam P. Dale • Rafeh Khan • Anup Mathew • Naomi O. Hersey • Robert Peck • Frederick Lee Stephen D. Goode



Received: 21 September 2014 / Accepted: 19 January 2015 Ó Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2015

Abstract Purpose PTC and stenting procedures are associated with significant risks including life-threatening haemorrhage, sepsis, renal failure and high mortality rates. PTC tract closure methods are utilised to reduce haemorrhagic complications despite little evidence to support their use. The current study assesses the incidence of haemorrhagic complications following PTC and stenting procedures, both prior to and following the introduction of a dedicated expanding gelatin foam-targeted embolisation liver tract closure technique. Materials and Methods Haemorrhagic complications were retrospectively identified in patients undergoing PTC

A. P. Dale Department of Medical Microbiology, Basingstoke and North Hampshire Hospital, Aldermaston Road, Basingstoke, Hampshire RG24 9NA, UK e-mail: [email protected] R. Khan  A. Mathew  N. O. Hersey  R. Peck  F. Lee Department of Radiology, Northern General Hospital, Herries Road, Sheffield S5 7AU, UK e-mail: [email protected] A. Mathew e-mail: [email protected]

procedures both prior to (subgroup 1) and following (subgroup 2) the introduction of a dedicated targeted liver tract closure method between 9/11/2010 and 10/08/2012 in a single tertiary referral centre. Mean blood Hb decrease following PTC was established in subgroups 1 and 2. Kaplan–Meier life-table analysis was performed to compare survival outcomes between subgroups using the log-rank test. Results Haemorrhagic complications were significantly reduced following the introduction of the targeted PTC tract closure method [(12 vs. 3 % of subgroups 1 (n = 101) and 2 (n = 92), respectively (p = 0.027)]. Mean blood Hb decrease following PTC was 1.40 versus 0.68 g/dL in subgroups 1 and 2, respectively (p = 0.069). 30-day mortality was 14 and 12 % in subgroups 1 and 2, respectively. 50 % of the entire cohort had died by 174 days post-PTC. Conclusion Introduction of liver tract embolisation significantly reduced haemorrhagic complications in our patient cohort. Utilisation of this method has the potential to reduce the morbidity and mortality burden associated with post-PTC haemorrhage by preventing bleeding from the liver access tract. Keywords Embolization  Bile duct  Stent  Haemorrhage  PTC  Liver tract embolisation

N. O. Hersey e-mail: [email protected] R. Peck e-mail: [email protected]

Introduction

F. Lee e-mail: [email protected]

Percutaneous transhepatic cholangiography (PTC) is a radiological procedure that enables the transhepatic deployment of a stent or external drain within the biliary tree to relieve an obstructed system. The majority of PTC procedures are performed in patients with malignant disease and are palliative in a large number of cases. Relief of

S. D. Goode (&) Sheffield Vascular Institute, Northern General Hospital, Herries Road, Sheffield S5 7AU, UK e-mail: [email protected]

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A. P. Dale et al.: Liver Tract Embolisation Post-PTC

biliary obstruction following stent placement provides symptomatic relief and reduces the risk of sequelae and mortality associated with biliary stasis [1]. Furthermore, PTC and stenting allows for optimisation of hepatic function prior to surgical resection, chemotherapy or radiotherapy [2]. Despite the success of PTC procedures in relieving biliary obstruction, these procedures are associated with significant risks including haemorrhage, sepsis, renal failure and high mortality rates for both malignant and benign disease [3, 4]. The recently published British Society of Interventional Radiology (BSIR) Biliary Drainage and Stenting Registry (BDSR) presented a post-PTC haemorrhage rate of 6.1 % [3]. In the same publication, overall post-PTC inpatient mortality was 19.2 % (19.8 % for malignant disease vs. 15.6 % for benign disease); however, mortality rates were significantly higher in patients solely undergoing drainage versus those undergoing combined drainage and stenting (25.1 vs. 17.3 %, respectively. p = 0.03). The BDSR also presented data on liver tract embolisation following PTC and demonstrated a trend towards decreased haemorrhagic complications in patients undergoing tract embolisation. The specific type of embolisation was not recorded but these data would suggest improvements in patient outcomes following liver tract embolisation. Reported methodologies for liver tract closure include coils, gelatin foam, amplatzer plugs, avitene or glue [5–8]. Other benefits to tract embolisation were presented by Lyon et al. showing decreased post-procedural pain and analgesia usage [9]. Arterial haemorrhagic complications occur in 1.9–2.2 % following percutaneous biliary drainage procedures and as a result of rapid intravascular volume depletion, and are often clinically evident soon after the procedure [10, 11]. While evidence relating to the incidence of arterial bleeding is clear, there is a sparsity of data relating to haemorrhage originating from other sources, e.g. the hepatic or portal venous systems. Only once the total scope of all haemorrhagic complications is identified, will the true burden of bleeding following transhepatic interventions be known. The aim of our work was to assess the incidence of all haemorrhagic complications following PTC and stenting procedures in our institution, both before and after the routine introduction of a dedicated expanding gelatin foamtargeted embolisation liver tract closure technique.

Materials and Methods Patient Selection The electronic radiology department database was retrospectively interrogated to identify patients undergoing PTC

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and stent procedures between 9/11/2010 and 10/08/2012. Patients undergoing PTC alone or PTC with external biliary drain placement were excluded. Tract embolisation using the Hunter Biopsy Sealing DeviceÒ to deliver targeted expandable gelatin foam pledgets into the liver tract was introduced on 26/07/2011. The cohort was divided into two subgroups, i.e. patients undergoing PTC and stent procedures prior to (subgroup 1) and following (subgroup 2) the introduction of dedicated PTC tract embolisation. The study was approved by the authors’ NHS Trust Clinical Effectiveness Unit. Data were collected in an anonymised database to ensure patient confidentiality. No additional tests were carried out for the purpose of this study, i.e. all testing was part of the routine clinical care/ investigation of each patient. Data Collection Demographic data including patient sex, age, presenting diagnosis, along with pre- and post-PTC blood haemoglobin (Hb) concentration data were collated. Procedural data collection related to lobe of puncture, sheath size (French), stent details (e.g. covered or uncovered and stent length) and embolisation data. Data relating to long-term post-PTC patient outcomes were collated to ascertain long-term survival in the individual subgroups and the entire cohort. All the PTC and stenting procedures were performed by a Consultant Interventional Radiologist directly or by a senior Interventional Radiology Trainee supervised directly by a Consultant Interventional Radiologist. Technical Details Assessment of baseline blood parameters including clotting profile, full blood count and renal function was performed prior to PTC in all cases. Coagulopathy was corrected pre-procedure using intravenous (IV) vitamin K. IV antibiotic prophylaxis was administered and continued following PTC if cholangitis was suspected clinically. Subgroup 1 underwent PTC with stent insertion (without balloon dilatation) under local anaesthetic and conscious sedation. Peripheral intrahepatic bile duct puncture was performed under ultrasound (US) avoiding visible blood vessels. At the end of the procedure following successful stent deployment, the sheath left in situ was withdrawn from the bile duct into the liver parenchyma and the sidearm tap was assessed for any evidence of haemorrhage. If no haemorrhage was present, the sheath was removed. If there was evidence of haemorrhage, then the sheath remained in situ for 5 min to enable formation of an autologous blood clot within the liver tract. If following

A. P. Dale et al.: Liver Tract Embolisation Post-PTC

this there was continued bleeding, then tract embolisation maybe performed with coils or gelatine foam slurry. Subgroup 2 had the same methodology for the PTC and stent insertion as subgroup 1. However, at the end of the procedure, embolisation of the liver tract was routinely performed using an expandable gelatin foam pledget (Hunter Biopsy Sealing Device, Vascular Solutions, MO, USA). The procedural steps utilised for this targeted embolisation technique, which enables the liver tract to be filled with expanding gelatin foam to prevent haemorrhage or bile leak, are outlined in Fig. 1. The Hunter Biopsy Sealing Device is designed to facilitate haemostasis following percutaneous liver biopsy procedures. There are four radial-compressed gelatine foam pledgets within the pack. One radially compressed gelatin foam pledget made from absorbable gelatin sponge has a radiopaque tantalum tip. This allows the material to be visible under fluoroscopic imaging. The remaining three pledgets, which contain no radiopaque material, are used to help maintain the location of the initial radiopaque pledget and facilitate haemostasis within the biopsy tract. Each radially compressed gelatin foam pledget is 2 cm in length and expands to 1 cm diameter once fully hydrated. The pledgets are sized for needle gauge rather than for sheath size, but a 14 g pledget will fit a 6 fr sheath. Initially, the gelatin foam pledgets are introduced into the vascular sheath and then advanced using a push rod stylet (Fig. 1A–E). On average, two pledgets were used; however, sometimes three were required for a deep bile duct puncture. The first pledget advanced has a radiopaque marker, and after withdrawing the sheath to the bile duct access point, the radiopaque marker is positioned directly at the access point thus filling and expanding into the tract left in the liver by the sheath (Fig. 1F). The sheath is then withdrawn over the pledgets as they are stabilised in position by maintaining forward pressure on the push rod stylet (Fig. 1G). If following the delivery of two pledgets there was still some liver parenchyma unfilled, a third pledget would be introduced.

Quantification of Haemorrhagic Complications Haemorrhagic complications were subdivided into two main categories including (a) identifiable haemorrhage, where a haemorrhagic source was evident on clinical examination or radiological investigation following PTC; (b) patients with PTC-related haemorrhage requiring blood transfusion up to 10 days post-procedure. Pre-PTC Hb concentrations (g/dL) were compared with a 10-day postprocedure mean Hb (g/dL) for each patient. This allowed for quantification and comparison of blood loss post-PTC in both subgroups 1 and 2.

Statistical Analysis Statistical analysis was carried out using SPSSÒ version 19.0 (IBM, New York, Armonk, USA). Statistical significance was set as p \ 0.05. The v2 test and t test were used for analysis of categorical and continuous data, respectively. Kaplan–Meier life-table analysis was performed to compare survival outcomes between subgroups using the log-rank test.

Results Demographics Baseline variables including age, sex and incidence of malignant diagnoses did not differ significantly between patients in subgroups 1 (n = 101) and 2 (n = 92) (see Table 1). Variation in procedural specifics including number of lobe puncture attempts, use of covered versus non-covered stents, and stent length and sheath size (Fr) are outlined in Table 2. In subgroup 2, there was a significant increase in sheath size used and also an increase in the proportion of covered stents being used that need larger sheath sizes for delivery. Clinical Outcomes Haemorrhagic complications were significantly reduced following the introduction of targeted expanding gelatin foam pledget tract closure and occurred in 12 versus 3 % of subgroups 1 and 2, respectively (p = 0.027) (see Table 3). A strong trend towards significant reduction in identifiable haemorrhage [6 vs. 1 %, subgroups 1 and 2, respectively (p = 0.074)] and requirement for blood transfusion postPTC [10 vs. 3 %, subgroups 1 and 2, respectively (p = 0.069)] was also observed (see Table 4 for further details relating to patients with identifiable haemorrhage). Radiologically guided vascular embolisation was required on one occasion to ensure haemostasis. A significant decrease in pre- versus post-PTC blood Hb concentrations was observed in the entire cohort (11.6 prePTC vs. 10.5 g/dL post-PTC. p = 0.001). There was a strong trend towards a significant reduction in blood Hb decrease pre- versus post-PTC on comparing subgroups 1 and 2; however, this difference did not reach statistical significance (mean decrease in blood Hb of 1.40 and 0.68 g/dL in subgroups 1 and 2, respectively (p = 0.069). Survival Outcomes 30-day mortality figures were not significantly different between subgroups 1 and 2 (14 vs. 12 %, respectively) (see

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A. P. Dale et al.: Liver Tract Embolisation Post-PTC Fig. 1 Technical details of pledget delivery method

A Pledgets and pusher

B Pledgets introduced into sheath

C Pledgets advanced down sheath

D Sheath in bile ducts and radiopaque marker of pledget seen in sheath

E Sheath withdrawn to access point to bile duct and pledgets advanced

F Sheath withdrawn further and pusher advancing and stabilising pledgets in liver tract

G 2 x pledgets successfully deployed into liver tract with radiopaque tip visible at entry point to bile ducts

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A. P. Dale et al.: Liver Tract Embolisation Post-PTC Table 1 Demographic details of subgroups 1 and 2 Subgroup 1 (n = 101)

Subgroup 2 (n = 92)

p value

71

70

ns

Male

58

44

ns

Female

43

48

ns

90

86

ns

Age (years) Sex (%)

Malignant disease (%)

ns non-significant, Subgroup 1 pre-introduction of PTC gelatin foam pledget tract closure, Subgroup 2 post-introduction of PTC gelatin foam pledget tract closure Table 2 Procedural details Subgroup 1 (n = 101)

Subgroup 2 (n = 92)

p value

Single lobe puncture

91

90

ns

Covered stent (%)

38

56

0.039

Mean stent length (cm)

6.4

6.9

0.165

Sheath French size (median)

7

8

0.03

For covered stents (Taewoong, EGIS or Boston), 8 or 9 fr sheaths were utilised. For benign disease, uncovered Boston wallstents were also utilised (6 fr sheath) ns non-significant, Subgroup 1 pre-introduction of PTC tract closure, Subgroup 2 post-introduction of PTC tract closure

Fig. 2). 50 % of the entire cohort had died by 174 days post-PTC (see Fig. 3). Figure 4 shows long-term survival for patients with benign versus malignant disease.

Discussion Haemorrhagic complications following PTC include haemobilia, peri-hepatic haematoma formation, haemoperitoneum and direct blood loss into an externally placed biliary drain. Haemorrhage secondary to arterial injury or in patients with portal hypertension, where bleeding frequently originates from peri-hepatic or abdominal wall venous collaterals, can prove difficult to control [12]. In cases of arterial injury, prompt vascular embolisation is often required to prevent massive and potentially fatal haemorrhage [4, 13, 14]. The incidence of arterial haemorrhage following PTC procedures ranges from 1.6 to 2.3 % [4–6, 10]. However, historically, the incidence of haemobilia following percutaneous biliary drainage procedures originating from both arterial and venous sources has been reported to be as high as 13.8 % [15]. In the recent BDSR that monitored modern-day practice, haemorrhagic complications occurred in 6.1 % [3]. Although results from this study must be interpreted with caution as data entry was voluntary, the high bleeding incidence observed is likely explained in part by the lack of experience amongst interventional radiologists performing these procedures. This is evidenced by the high ratio of radiologists to total number procedures performed in this cohort.

In the current study, haemorrhagic complications occurred in 12 % of patients undergoing PTC and stenting procedures prior to the introduction of targeted liver tract embolisation using expandable gelatin foam pledgets. Following the introduction of the dedicated transhepatic tract embolisation methodology, haemorrhagic complications were reduced significantly to 3 %. In addition, we observed a significant decrease in post-PTC Hb drop. Our data suggest a spectrum of bleeding complications, ranging from severe arterial haemorrhage to slower low-pressure venous bleeding or self-limiting arterial bleeding resulting in a less striking decrease in haemoglobin concentration post-procedure. It may be that tract closure helps to prevent intrahepatic, subcapsular and intraductal bleeding from arterial, venous and portal venous sources. Although we had a relatively small number of patients in each subgroup, we did demonstrate a trend (non-significant) towards improved 30-day mortality following the introduction of the targeted liver tract embolisation, suggesting a potential benefit. However, our study had limited numbers and this finding did not reach statistical significance. Despite a poor evidence base, PTC tract closure methods including the delivery of gelatin foam or the use of coil embolisation or avitene have been adopted by some operators. In a recent study by Uller et al., gelfoam was demonstrated to be both safe and effective when utilised to close transhepatic and trans-splenic puncture tracts [16]. Only 12 % of PTC procedures in the BDSR report series involved the use of a dedicated tract closure method. Despite a trend towards reduced incidence of haemorrhage in

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A. P. Dale et al.: Liver Tract Embolisation Post-PTC Table 3 Haemorrhagic complications in subgroups 1 and 2 Haemorrhagic complication category

Subgroup 1 (n = 101)

Subgroup 2 (n = 92)

p value

Identifiable haemorrhage

6 % (n = 6)

1 % (n = 1)

0.074

Requirement for blood transfusion

10 % (n = 10)

3 % (n = 3)

0.06

Combined haemorrhagic complicationsa

12 % (n = 12)

3 % (n = 3)

0.027

a

Combined haemorrhagic complications category include patients with requirement for blood transfusion, identifiable haemorrhage or both requirement for blood transfusion and identifiable haemorrhage

Table 4 Details for individuals with identifiable haemorrhage post-PTC Patient number

Subgroupa

Identifiable haemorrhage details

Blood transfusion

Survival (days post-PTC)

Vascular embolisation

Post-PTC blood Hb decrease (%)b

1

1

Haemorrhage from liver puncture site

No

823 (alive)

No

13.5 %

2

1

Active contrast extravasation on CT from left lobe puncture site

Yes

0 days (died)

Yes

42 %

3 4

1 1

Haemobilia and haemoperitoneum on CT scan Frank haemobilia at end of procedure

Yes No

623 (died) 352 (died)

No No

36.9 % na

5

1

Haemorrhage in liver and capsule rupture and haemoperitoneum

Yes

45 days (died)

No

34 %

6

1

Large haemoperitoneum and extravasation from right lobe puncture site

Yes

3 (died)

No

44 %

7

2

Large right haemothorax, no intra-peritoneal blood, thoracotomy required

Yes

17 (died)

No

20 %

a

Subgroup 1 pre-introduction of PTC tract closure, Subgroup 2 post-introduction of PTC tract closure

b

Post-PTC decrease in blood Hb (g/dL) = pre-PTC Hb—10 day post-PTC average Hb (g/dL) expressed as percentage decrease in blood Hb

Fig. 2 Kaplan–Meier survival curve for entire cohort (subgroups 1 and 2 combined)

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Fig. 3 Kaplan–Meier survival curve (subgroup 1 vs. subgroup 2)

A. P. Dale et al.: Liver Tract Embolisation Post-PTC

Fig. 4 Kaplan–Meier survival curve (malignant vs. benign disease)

these patients, this association did not reach statistical significance [3]. There was no mention of the nature of the tract embolisation in the registry. The BDSR also presented data demonstrating a significant reduction in mortality for patients undergoing biliary stenting versus biliary drainage (25.1 vs. 17.3 %, respectively, p = 0.03). This is an important distinction as being able to perform a biliary stenting procedure in a single episode is more beneficial for the patient and tract embolisation and closure is an essential part of this. Quality improvement guidelines published by the Society of Interventional Radiology suggest a threshold of 5 % for post-PTC haemorrhagic complications and outline specific criteria to define minor and major haemorrhage [17]. In the current analysis, we not only identify all haemorrhagic complications of clinical significance but also demonstrate that, amongst the entire cohort (n = 193), there was a statistically significant decrease in pre- versus post-PTC blood haemoglobin concentrations. This evidence suggests that while only the minority experience clinically significant haemorrhage, a much larger proportion experience subclinical haemorrhage not requiring clinical intervention. Interestingly, a trend towards a significant reduction in blood Hb decrease was observed following the introduction of the targeted liver tract embolisation methodology suggesting that this technique reduced blood loss across the board in this patient cohort. There was a learning curve for utilising this novel methodology for transhepatic liver tract embolisation. Initial methods used the smaller gelatin foam pledgets (20 gauge), and in a number of cases failed to prevent

haemorrhagic complications. CT scan follow up in these cases revealed the gelatin foam pledget with the tantalum tip to be located outside the liver parenchyma, presumably as a result of bleeding-related displacement as it was too small to fit the liver tract. On identifying this initial flaw, we moved to using the larger pledget sizes, i.e. 14 gauge (please note that the Hunter system is sized for gauge not sheath and for biopsy tract sealing not PTC biliary procedures). Data presented in this paper relate to cases where the 14 gauge pledgets were used, which provided the most tract embolisation and radial filling. Essentially, the embolic material used needs to be of sufficient size to fill and expand into the liver tract to ensure adequate embolisation. Consequently, our methodology was adapted to ensure that the site of transhepatic biliary access was marked with a fluoroscopic image, thus ensuring accurate placement of the pledgets on tract closure. There were also some early difficulties with left lobe tract embolisation due to the angle of access to the bile duct which is not perpendicular to the X-ray beam when in an AP orientation given the anterior location of the left lobe and anterior angulation of the bile ducts. In these cases, delivery of the pledget was occasionally suboptimal and often outside the liver capsule. The solution to this problem involved moving the image intensifier into a more right anterior oblique projection, allowing for better perpendicular visualisation of pledget delivery and thus accurate placement. A significant increase in the size of the delivery sheath was demonstrable in the post-embolisation group (subgroup 2). Although theoretically this should increase the risk of haemorrhagic complications, we still observed a significant decrease in haemorrhagic complications in subgroup 2. The increase in sheath size represents the move in our institution from the use of uncovered biliary stents to covered biliary stents, which require a larger sheath size for delivery [18]. This move had been made in an attempt to improve outcomes for biliary stenting by reducing the effects of tumour ingrowth through uncovered stents and to improve long-term patency. These tract embolisation methods could be further refined and utilised for other transhepatic access procedures, e.g. portal vein embolisation or for other transhepatic procedures where favourable results have previously been reported [19, 20]. Study limitations included relatively small numbers of patients in each subgroup. Larger numbers of patients may have provided the power required to confirm or refute any reduction in mortality shown between subgroups 1 and 2. There were also limitations on the pledgets used for embolisation. In particular, they are sized for gauge not sheath size, and are short in length resulting in the need to use numerous pledgets to fill the tract. In addition, the gelfoam pledget used was not licenced for PTC and biliary work. There is definitely scope to improve the current gelatin

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A. P. Dale et al.: Liver Tract Embolisation Post-PTC

foam pledget design to enable an improved and more robust embolisation technique. In the majority of cases, PTC and stenting procedures are palliative. Mortality data from the current study support the observations of previous authors [21, 22] and demonstrate poor life expectancy in this patient group. Although PTC and stenting itself provides symptom relief and extends life, the importance of reducing procedure-associated complications cannot be understated as it has the potential to improve quality of life. The consequences of major procedure-related haemorrhage are clear; however, the extent of subclinical bleeding identified in this study should not be ignored as it also has the potential to cause significant adverse sequelae. Methods to prevent post-PTC haemorrhage are therefore extremely important and should continue to be developed to reduce the morbidity and mortality burden associated with these transhepatic interventions.

8. 9.

10.

11.

12. 13.

14.

Conflict of interest Adam P. Dale, Rafeh Khan, Anup Mathew, Naomi O. Hersey, Robert Peck, Frederick Lee and Stephen D. Goode declare that they have no conflict(s) of interest.

15.

Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects.

16.

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17.

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Hepatic Tract Plug-Embolisation After Biliary Stenting. Is It Worthwhile?

PTC and stenting procedures are associated with significant risks including life-threatening haemorrhage, sepsis, renal failure and high mortality rat...
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