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Early View Article: Online published version of an accepted article before publication in the final form.

Journal Name: International Journal of Hepatobiliary and Pancreatic Diseases (IJHPD)

Type of Article: Case Report

Title: Migration of an uncovered self-expandable metal biliary stent in a patient with inoperable cholangiocarcinoma: A case report

Authors: Edward Robert John Walton, Ewan Simpson, Mark Callaway

doi: To be assigned

Received: 14th November 2014

Accepted: 10th December 2014

How to cite the article: Walton ERJ, Simpson E, Callaway M. Migration of an uncovered self-expandable metal biliary stent in a patient with inoperable cholangiocarcinoma: A case report. International Journal of Hepatobiliary and Pancreatic Diseases (IJHPD). Forthcoming 2015.

Disclaimer: This manuscript has been accepted for publication. This is a pdf file of the Early View Article. The Early View Article is an online published version of an accepted article before publication in the final form. The proof of this manuscript will be sent to the authors for corrections after which this manuscript will undergo content check, copyediting/proofreading and content formatting to conform to journal’s requirements. Please note that during the above publication processes errors in content or presentation may be discovered which will be rectified during manuscript processing. These errors may affect the contents of this manuscript and final published version of this manuscript may be extensively different in content and layout than this Early View Article.

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TYPE OF ARTICLE: Case Report 1

2

TITLE: Migration of an uncovered self-expandable metal biliary stent in a patient with 3

inoperable cholangiocarcinoma: A case report 4

5

AUTHORS: 6

Edward Robert John Walton1, Ewan Simpson2, Mark Callaway3 7

8

AFFILIATIONS: 9 1(MbChB FRCR), University Hospitals Bristol, Radiology Department, Bristol Royal 10

Infirmary, Upper Maudlin Street, Bristol, United Kingdom, BS2 8HW. Email ID: 11

edwardwalton@hotmail.co.uk 12 2(MBBS FRCR), University Hospitals Bristol, Radiology Department, Bristol Royal 13

Infirmary, Upper Maudlin Street, Bristol, United Kingdom, BS2 8HW. Email ID: 14

ewan.simpson@nbt.nhs.uk 15 3(MRCP FRCR), University Hospitals Bristol, Radiology Department, Bristol Royal 16

Infirmary, Upper Maudlin Street, Bristol, United Kingdom, BS2 8HW. Email ID: 17

mark.callaway@UHBristol.nhs.uk 18

19

CORRESPONDING AUTHOR DETAILS 20

Dr. Edward Robert John Walton, 21

University Hospitals Bristol, Radiology Department, Bristol Royal Infirmary, Upper 22

Maudlin Street, Bristol, United Kingdom, BS2 8HW. 23

Phone No: 07752510574 24

Email ID: edwardwalton@hotmail.co.uk 25

26

Short Running Title: Migration of biliary USEMS 27

28

Guarantor of Submission : The corresponding author is the guarantor of 29

submission. 30

31

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TITLE: Migration of an uncovered self-expandable metal biliary stent in a patient with 32

inoperable cholangiocarcinoma: A case report 33

34

ABSTRACT 35

Migration of plastic and covered-metal stents is a recognised phenomenon but is an 36

extremely uncommon complication of uncovered self-expandable metal stents 37

(USEMS). To our knowledge, this is the first case report describing the migration of a 38

USEMS used to treat proximal biliary obstruction secondary to cholangiocarcinoma. 39

This report outlines the complications surrounding this case and discusses the 40

existing literature and the potential complications of uncovered and covered self-41

expandable metal stents. 42

43

Keywords: Biliary, uncovered self-expanding metal stent, migration, 44

cholangiocarcinoma 45

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TITLE: Migration of an uncovered self-expandable metal biliary stent in a patient with 63

inoperable cholangiocarcinoma: A case report 64

65

INTRODUCTION 66

Biliary stenting is an established treatment option for obstruction of the biliary tree. A 67

randomised control trial by Andersen et al [1] suggested that endoprothesis 68

placement is associated with lower total mortality, lower major complications and a 69

reduction in total hospital stay when compared to surgery. 70

Biliary stents can be broadly divided into plastic or metal. Plastic stents are available 71

in a variety of materials, lengths, and designs. Modern metal stents are commonly 72

self-expandable (SEMS) and can be uncovered (USEMS) or may be partially or fully 73

covered (CSEMS). The type of stent selected depends on the aetiology of the 74

obstruction and on patient factors. Because SEMS are more likely to remain patent 75

for longer than plastic stents, they are recommended for palliation of malignant hilar 76

strictures where life expectancy is over three months. 77

We present the case of a 52 year old woman with hilar cholangiocarcinoma causing 78

jaundice that underwent palliative stenting with an USEMS. The case was 79

complicated by distal migration resulting in re-obstruction necessitating repeat 80

intervention. Stent migration is a recognised complication with both plastic stents and 81

CSEMS. It is seen extremely uncommonly with USEMS, and to our knowledge this is 82

the first case report to describe migration of a USEMS in a proximal biliary 83

obstruction. The advantages and disadvantages of various types of stents used for 84

biliary obstruction and risk factors for stent migration are discussed. 85

86

CASE REPORT 87

A 52 year old woman presented to her G.P with a four month history of right upper 88

quadrant discomfort and was referred for an out-patient abdominal ultrasound scan. 89

This revealed intrahepatic duct dilatation and subsequent computed tomography 90

[CT] of the liver and magnetic resonance cholangiopancreatography [MRCP] 91

confirmed imaging features of a 24mm intrahepatic cholangiocarcinoma. This was 92

located immediately proximal to the confluence of the left and right hepatic ducts and 93

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was causing obstruction of the left intrahepatic ducts. There were no distant 94

metastases identified on imaging or staging laparoscopy. 95

Endoscopic retrograde cholangiopancreatography [ERCP] and direct endoscopy of 96

the bile duct was performed with the aim of directly visualising the tumour to obtain a 97

biopsy and confirm the diagnosis. Cannulation of the bile duct was difficult and a pre-98

cut sphincterotomy was performed in an attempt to facilitate access, but this was 99

unsuccessful. The procedure was complicated by a duodenal perforation with 100

retroperitoneal collection and pancreatitis, which delayed definitive management. 101

The tumour was thought to be resectable after initial imaging, but unfortunately, 102

repeat CT demonstrated progression over the subsequent weeks with involvement of 103

the right portal vein and right intrahepatic ductal system. 104

The patient was discharged two weeks after the ERCP, but re-presented to the 105

emergency department a week later complaining of abdominal pain and nausea. At 106

this time she was noted to be clinically jaundiced. Fluoroscopically guided 107

percutaneous trans-hepatic cholangiography (PTC) and bare metal stent insertion 108

was therefore performed under conscious sedation as a palliative procedure to 109

relieve the obstruction. Following puncture of the right anterior ducts with an 110

introducer set ('Accustick' introducer set, Boston scientific®), complete occlusion of 111

the ductal system was demonstrated. There was no cross filling of the left segmental 112

ducts. The obstruction was traversed with a guide wire. A 10mm x 70mm uncovered 113

self expandable metal stent (Placehit Biliary WALLSTENT, Boston Scientific®) was 114

then deployed across the stricture and was positioned with 3 cm of stent proximal to 115

the tumour to allow maximum proximal expansion within the duct and ensure optimal 116

flow of bile from the intrahepatic ducts (Figure 1). Free flow of contrast into the 117

common bile duct was demonstrated, indicating successful procedure and no 118

balloon expansion was required. 119

The day after the procedure, the patient complained of abdominal pain and nausea, 120

and developed a temperature of 38.5°. She was noted to be more jaundiced. Serum 121

bilirubin rose from 84 umol/L (normal range: 21-100 umol/L) before the stent 122

placement to 268 umol/L two days post-procedure. Full blood count revealed 123

elevated white cell count of 21 X109/l [normal range: 4-11X109/l] and serum C-124

reactive protein (CRP) increased to 47mg/l (normal range: 4-8mg/l). A diagnosis of 125

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biliary sepsis was made. Blood cultures grew Enterococcus faecium with resistance 126

to Amoxicillin. Teicoplanin, Gentamycin and Metronidazole were commenced. The 127

liver function tests failed to improve over the next few days, and a repeat PTC was 128

performed 8 days after the first procedure which demonstrated that the stent had 129

slipped through the stricture into the extra-hepatic biliary tree, and that the right 130

intrahepatic duct was once again completely occluded (Figure 2). A wire was placed 131

across the occlusion and through the centre of the migrated stent, and a further 132

uncovered 10mm x 70mm self expandable metal stent (Placehit Biliary 133

WALLSTENT, Boston Scientific®) was then placed across the stricture and 134

deployed, the distal end of the new stent sited within the proximal end of the 135

migrated one. There was some waisting in the region of the tumour which was 136

dilated using a balloon dilatation catheter (35LP Low-Profile PTA Balloon Dilatation 137

Catheter (0.35", 8mm diameter 4cm length). There was subsequent free flow of 138

contrast into the duodenum indicating a successful procedure (Figure 3). 139

Following the placement of the second stent, the patient improved with reduction in 140

pain and nausea. Serum bilirubin dropped from 195 uml/L to 119 umol/L within two 141

days, and she was discharged four days later for out-patient oncology follow up. 142

143

DISCUSSION 144

Plastic vs Self-expandable metal biliary stents: 145

Compared with standard 10f plastic stents, 10mm self-expandable metal stents 146

(SEMS) have an approximately 3 times greater transverse diameter which makes 147

biliary obstruction less likely. One Cochrane review paper found no difference in 148

technical success, therapeutic success, procedural complications or 30-day mortality 149

between metal and plastic stents but found that metal stents lead to significantly less 150

episodes of recurrent biliary obstruction, and reduced re-intervention rates [2]. A 151

more recent meta-analysis comparing plastic vs metal stents found a longer patency, 152

lower re-intervention rate, and longer mean survival in biliary obstruction treated with 153

metal stents when compared to plastic stents [3]. This study also conducted a 154

subgroup analysis comparing hilar vs distal biliary obstruction and reported a higher 155

chance of stent occlusion in hilar obstruction, suggesting the use of a metal stent is 156

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preferable in these cases. Neither study looked specifically at the risks of stent 157

migration. 158

Covered vs Uncovered Self-expandable Metal Stents 159

A number of factors may contribute to SEMS failure including tumour ingrowth, 160

epithelial hyperplasia, and occlusion caused by debris or clot. This led to the 161

development of covered SEMS which have a membrane that is intended to prevent 162

penetration of cellular material through the stent wall. A meta-analysis of 163

randomised controlled trials comparing covered self-expandable metal stents 164

(CSEMS) versus uncovered (USEMS) found that CSEMS were associated with 165

significantly prolonged stent patency (weighted mean difference [WMD] 60.56 days; 166

95% confidence interval [CI], 25.96, 95.17; I² = 0%) and longer stent survival (WMD 167

68.87 days; 95% CI, 25.64, 112.11; I[2] = 79%). However, tumour overgrowth, 168

sludge formation and – most significantly - stent migration were higher with CSEMS 169

(relative risk [RR] 2.02; 95% CI, 1.08, 3.78; I² = 0%), (RR 2.89; 95% CI, 1.27, 6.55; I² 170

= 0%) (RR 8.11; 95% CI, 1.47, 44.76; I² = 0%), [4]. 171

It is well known that USEMS are extremely unlikely to migrate [5]. A randomised 172

controlled trial comparing CSEMS versus USEMS by Telford et al [6] enrolled 129 173

patients between 2002 and 2008 and randomised patients into USEMS and CSEMS 174

arms. There was significantly more stent migration in the covered group with 8 (12%) 175

of the covered stents migrating compared with none of the uncovered stents (P.006). 176

This however was principally for distal biliary strictures. In a prospective trial by 177

Kullman et al [7] 400 patients were randomized to CSEMS or USEMS. Stent 178

migration occurred in 6 patients in the covered group versus no patients in the 179

uncovered group. A retrospective review of 749 SEMS cases by Lee et al [8] for 180

distal biliary tract obstruction (578 USEMS and 171 CSEMS) found only 3 cases of 181

migration in the USEMS group (0.5%) and 12 cases (7%) in the CSEMS group. 182

Risk factors for stent migration: 183

Risk factors for migration of USEMS are not known as the numbers previously 184

reported are so small. However, there have been recent publications on the risks for 185

migration of plastic stents and CSEMS. Yoshiaki Kawaguchi et al [9] recently 186

assessed the outcomes of 396 patients with bile duct stenosis who had undergone 187

endoscopic plastic stent placement for a variety of indications (the majority for 188

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benign obstruction such as stones in the biliary tree), and found that distal biliary 189

strictures and common bile duct diameters greater than 10mm were risk factors for 190

stent migration. They also found an increased risk of migration of straight plastic 191

stents when compared with pigtail stents. A recent retrospective analysis of CSEMS 192

migration conducted by Nakai et al [5] analysed a number of patient and stent factors 193

in 290 patients who had a CSEMS for distal biliary obstruction due to pancreatic 194

malignancy. Stent migration rate was 15.2%, and significant risk factors for stent 195

migration included chemotherapy, low radial force, and duodenal invasion by the 196

pancreatic tumour. 197

Neither of these studies are directly relevant to our case in which an uncovered self-198

expandable metal stent was deployed in a proximal location for a malignant stricture. 199

Our patient underwent a sphincterotomy at ERCP to facilitate access, and had not 200

had chemotherapy at time of stenting. Balloon expansion was not performed at the 201

time of procedure. In their large retrospective review of 749 SEMS in malignant 202

biliary obstruction, Lee et al [8] postulate that CSEMS are more likely to migrate 203

because of their high axial force and because they do not embed in the adjacent 204

tissue. They also note that two out of the three USEMS patients who had migration 205

had undergone a sphincterotomy as was the case with our patient. However, it is 206

notable that all of their patients had a distal biliary obstruction due to pancreatic 207

malignancy, rather than proximal obstruction as in our case. Furthermore, previous 208

studies have failed to show a difference in the risk of stent migration in patients who 209

have undergone a biliary sphincterotomy [10] and balloon expansion is not always 210

required for self-expanding stents. There is no literature describing a difference in 211

patency or risk of migration between balloon expanded and non-balloon expanded 212

SEMS. 213

214

CONCLUSION 215

Radiologists and endoscopists must be familiar with the relative advantages and 216

disadvantages of the various types of stents available for relief of obstruction of the 217

biliary tree, which are dependent on the aetiology and location of the obstruction, the 218

duration that stent patency must be maintained for, and other patient factors. The 219

risk factors for stent migration in plastic stents and CSEMS described above may 220

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help when deciding on the most appropriate choice of stent and placement method. 221

However, it is well established that USEMS are extremely unlikely to migrate, and 222

the risk factors for stent migration with USEMS are not known. To our knowledge this 223

is the first case report to describe migration of USEMS inserted for biliary obstruction 224

caused by hilar cholangiocarcinoma. Further study of USEMS migration will help to 225

determine the contributing causes of this uncommon complication. 226

227

CONFLICT OF INTEREST 228

Author #1 No conflict of interest 229

Author #2 No conflict of interest 230

Author #3 No conflict of interest 231

232

AUTHOR’S CONTRIBUTIONS 233

Edward Robert John Walton 234

Group1 - Conception and design, Acquisition of data, Analysis and interpretation of 235

data 236

Group 2 - Drafting the article, Critical revision of the article 237

Group 3 - Final approval of the version to be published 238

Ewan Simpson 239

Group1 - Conception and design, Acquisition of data, Analysis and interpretation of 240

data 241

Group 2 - Drafting the article, Critical revision of the article 242

Mark Callaway 243

Group 2 - Drafting the article, Critical revision of the article 244

245

ACKNOWLEDGEMENTS 246

NONE 247

248

249

250

251

252

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REFERENCES 253

1. Andersen J, Sørensen S, Kruse A, Rokkjaer M, Matzen P. Randomised trial of 254

endoscopic endoprosthesis versus operative bypass in malignant obstructive 255

jaundice. Gut. 1989;30(8):1132-5. 256

2. Moss AC, Morris E, Mac Mathuna P. Palliative biliary stents for obstructing 257

pancreatic carcinoma. Cochrane Database System Rev.2006;2. 258

http://onlinelibrary.wiley.com/doi/10.1002/14651858.CD004200.pub4/pdf/stan259

dard. 260

3. Hong Wd, Chen Xw, Wu Wz, Zhu Qh, Chen Xr. Metal versus plastic stents for 261

malignant biliary obstruction: An update meta-analysis. Clinics and research 262

in hepatology and gastroenterology. 2013;37(5):496-500. 263

4. Saleem A, Leggett CL, Murad MH, Baron TH. Meta-analysis of randomized 264

trials comparing the patency of covered and uncovered self-expandable metal 265

stents for palliation of distal malignant bile duct obstruction. Gastrointestinal 266

endoscopy. 2011;74(2):321-7. 267

5. Nakai Y, Isayama H, Kogure H, Hamada T, Togawa O, Ito Y, et al. Risk 268

factors for covered metallic stent migration in patients with distal malignant 269

biliary obstruction due to pancreatic cancer. Journal of gastroenterology and 270

hepatology. 2014. 271

6. Telford JJ, Carr-Locke DL, Baron TH, Poneros JM, Bounds BC, Kelsey PB, et 272

al. A randomized trial comparing uncovered and partially covered self-273

expandable metal stents in the palliation of distal malignant biliary obstruction. 274

Gastrointestinal endoscopy. 2010;72(5):907-14. 275

7. Kullman E, Frozanpor F, Söderlund C, Linder S, Sandström P, Lindhoff-276

Larsson A, et al. Covered versus uncovered self-expandable nitinol stents in 277

the palliative treatment of malignant distal biliary obstruction: results from a 278

randomized, multicenter study. Gastrointestinal endoscopy. 2010;72(5):915-279

23. 280

8. Lee JH, Krishna SG, Singh A, Ladha HS, Slack RS, Ramireddy S, et al. 281

Comparison of the utility of covered metal stents versus uncovered metal 282

stents in the management of malignant biliary strictures in 749 patients. 283

Gastrointestinal endoscopy. 2013;78(2):312-24. 284

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9. Kawaguchi Y, Ogawa M, Kawashima Y, Mizukami H, Maruno A, Ito H, et al. 285

Risk factors for proximal migration of biliary tube stents. World journal of 286

gastroenterology: WJG. 2014;20(5):1318. 287

10. Güitrón A, Adalid R, Barinagarrementería R, Gutiérrez-Bermúdez J, 288

Martínez-Burciaga J. Incidence and relation of endoscopic sphincterotomy to 289

the proximal migration of biliary prostheses. Revista de gastroenterologia de 290

Mexico. 1999;65(4):159-62. 291

292

TABLES 293

NIL 294

295

FIGURE LEGENDS 296

Figure 1: Uncovered self-expandable metal stent has been deployed across the 297

stricture. The proximal aspect of the stent is shown at the confluence of the right 298

hepatic ducts (white arrow). Contrast material flows freely from the distal aspect of 299

the stent (black arrow), indicating successful procedure. 300

Figure 2: Right ductal system is once again obstructed. The stent has migrated from 301

its original position (white arrow) at the confluence of the right hepatic ducts, and 302

now lies beyond the stricture in the extrahepatic duct. 303

Figure 3: A second stent has been inserted, with proximal aspect well within a right 304

segmental duct (white arrow) and distal aspect within the proximal end of the 305

migrated stent (black broken arrow). Contrast material flows from the distal end of 306

the original stent (black solid arrow), indicating successful procedure. 307

308

309

310

311

312

313

314

315

316

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FIGURES 317

318

Figure 1: Uncovered self-expandable metal stent has been deployed across the 319

stricture. The proximal aspect of the stent is shown at the confluence of the right 320

hepatic ducts (white arrow). Contrast material flows freely from the distal aspect of 321

the stent (black arrow), indicating successful procedure. 322

323

324

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325

Figure 2: Right ductal system is once again obstructed. The stent has migrated from 326

its original position (white arrow) at the confluence of the right hepatic ducts, and 327

now lies beyond the stricture in the extrahepatic duct. 328

329

330

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331

Figure 3: A second stent has been inserted, with proximal aspect well within a right 332

segmental duct (white arrow) and distal aspect within the proximal end of the 333

migrated stent (black broken arrow). Contrast material flows from the distal end of 334

the original stent (black solid arrow), indicating successful procedure. 335