’Original article Self-expandable metal stent placement for malignant duodenal obstruction distal to the bulb Keith Wan Hang Chiua,c, Abdul Razacka and Anthony Maraveyasb Objective Self-expandable metal stents (SEMS) are widely used for the palliative management of malignant proximal gastroduodenal obstruction because of its low morbidity and mortality rates compared with surgical bypass. However, stent placement for duodenal obstruction beyond the first part of the duodenum is considered technically difficult and is not routinely performed. We report our experience with SEMS placement for these patients. Methods Between 2006 and 2015, 51 patients with unresectable or metastatic malignancy underwent SEMS placements under combined endoscopic and fluoroscopic guidance. Eighteen patients had intestinal obstruction distal to the duodenal bulb. Their demographics, technical and clinical outcomes, periprocedural morbidity and mortality, length of hospital stay, further interventions and overall survival were analysed. Results Out of the 18 cases, nine cases of intestinal obstruction were due to primary malignancy of the pancreas, three due to gastric malignancy, three from other locoregional cancers and three were the result of metastases. In 12 patients, the obstruction involved the second part (D2), in four the third part (D3) and in two the fourth part (D4) of the duodenum. A front-facing therapeutic gastroscope was used to visualize the duodenum before the stricture was crossed under direct vision and fluoroscopic guidance, with a catheter and guidewire, and a through-the-scope SEMS deployed using an ‘over-the-wire’ technique. Technical success rate was 89%. The mean gastric outlet obstruction scores improved from 0.63 to 2.57 (P < 0.0001). Four patients died within 30 days of the procedure, although none of the deaths were procedure related. The median length of postprocedural hospital stay was 4 days and the median overall survival was 58 days. Eur J Gastroenterol Hepatol 27:1466–1472 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

Introduction

Malignant gastroduodenal obstruction (GDO) occurs in up to 20% of patients suffering from advanced gastrointestinal malignancy, but it can also occur in patients with other locoregional cancers or metastases [1–5]. Patients often suffer from nausea, vomiting and pain, resulting in dehydration, malnutrition and deterioration in their quality of life. The inability to maintain nutrition is a particularly distressing symptom for patients and families in cancer management. Traditionally, these patients undergo surgical bypass to relieve their symptoms. Although open gastrojejunostomy has good clinical outcome, it is also associated with significant perioperative complications, morbidity and mortality [6–9]. The placement of self-expandable metal stents (SEMS) has been increasingly advocated because of their effectiveness and safety in the palliation of GDO [6,8,10–18]. However, European Journal of Gastroenterology & Hepatology 2015, 27:1466–1472 Keywords: duodenal obstruction, endoscopy, enteral feeding, palliative treatment, stents a Department of Radiology, Castle Hill Hospital, Hull and East Yorkshire NHS Trust, Cottingham, bThe Queen’s Centre for Oncology and Haematology, Hull and York Medical School, Castle Hill Hospital, Hull, UK and cDepartment of Diagnostic Radiology, The University of Hong Kong, Queen Mary Hospital, Hong Kong

Correspondence to Keith Wan Hang Chiu, FRCR, MBChB, Department of Diagnostic Radiology, The University of Hong Kong, Queen Mary Hospital, Room 406, Block K, Pok Fu Lam Road, Hong Kong Tel: + 44 148 287 5875; fax: + 44 148 267 5213; e-mail: [email protected] Received 22 June 2015 Accepted 11 August 2015

there is a perception that stenting beyond the duodenal bulb is technically challenging [19]. In this retrospective study, we describe our experience in a cohort of patients with GDO beyond the duodenal bulb with combined endoscopic and fluoroscopic techniques using a conventional gastroscope and an existing commercially available stent. Materials and methods

Over a 9-year period (2006–2015), 51 patients with symptomatic malignant duodenal obstruction underwent palliative SEMS insertion in Hull and East Yorkshire Hospitals NHS Trust, a tertiary referral centre in the UK. Eighteen of these patients had duodenal obstruction beyond the duodenal bulb and were included in this analysis. Outcomes measured include technical and clinical success, immediate periprocedural morbidity and mortality, changes in symptoms, length of hospital stay (LOS) post procedure, stent patency, further related reinterventions and overall survival (OS). Technical success is defined as successful deployment of the SEMS across the obstruction. Clinical success is defined as symptomatic relief and is measured by improvement in the standardized gastric outlet obstruction scoring system score: 0 = no oral intake, 1 = liquids only, 2 = soft solids and 3 = low-residue or full diet [1]. Periprocedural morbidity and mortality are events occurring within 24 h of the procedure. Reintervention is defined as any further procedure performed for recurrent

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DOI: 10.1097/MEG.0000000000000479

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obstructive symptoms, and stent patency is defined as the interval from stent insertion to stent occlusion, reintervention for recurring symptoms or death. Statistical analysis was carried out with the GraphPad Prism 6 statistical software package (GraphPad Software, La Jolla, California, USA). All 18 patients underwent radiological assessments (12 computed tomography scans, six water-soluble contrast studies) before the procedure. As recommended by international guidelines, a nasogastric (NG) tube (14 F Ryles tube) was routinely inserted at least 24 h before the procedure to empty and decompress the stomach, to reduce the risk of aspiration and avoid looping of the endoscope during the procedure. All procedures were performed under conscious sedation with intravenous fentanyl and midazolam. All the stents used were uncovered bare-metal EGIS Pyloric stents (S&G Bio, Seoul, Korea) with a diameter of 20 mm and a length of 12 cm. Where possible, the procedures were performed by two operators; the primary operator (A.R.), an interventional radiologist who is also fully trained in endoscopy, was responsible for navigating with the gastroscope as close to the stricture as possible, whereas the second operator (K.W.H.C. or other interventional radiologists) assisted and was responsible for negotiating through the stricture with catheters and guidewires using a ‘through-the-endoscope’ technique. SEMS were inserted using front-facing therapeutic gastroscopes with a 3.8 mm working channel (Pentax EG-3490k Video Gastroscope; Pentax Medical, Slough, UK). During the procedure, the gastroscope was first advanced as far as possible into the duodenum, and the duodenal obstruction was delineated with water-soluble contrast. The obstruction was then crossed with a hydrophilic guidewire (0.35 mm Terumo wire; Terumo, Tokyo, Japan) and a straight catheter (150 cm long, Slip-Cath Beacon Tip Catheter; COOK Medical, Bloomington, Indiana, USA) through the working channel. The straight catheter was used to cross the stricture ‘over-the-wire’ before the hydrophilic wire was removed, and watersoluble contrast was used to confirm satisfactory crossing of the stricture. In patients in whom the stricture could not be crossed using this method, a Dreamtone cannulating sphincterotome (Boston Scientific, Natick, Massachusetts, USA) was used as a catheter to aid with cannulation, as it provided angulation in the curve of the duodenum. Specific care was taken when manipulating this catheter to avoid cutting the tumour with the attached cutting wire. A stiff guidewire (500 cm Wallstent Super Stiff; Boston Scientific) was then placed through the catheter across the stricture, with the tip of the wire at least 10 cm distal to the obstruction. The catheter was then removed and a SEMS was introduced over the guidewire across the stricture using the ‘through-the-scope’ method and deployed across the stricture. Satisfactory deployment was confirmed using water-soluble contrast and/or by direct visualization (Fig. 1). Results

Baseline characteristics of the 18 patients are shown in Table 1. The second part of the duodenum was the most common site of obstruction because of pancreatic cancer (the most common cause). One patient in our cohort

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underwent two endoscopic decompressions of the stomach before duodenal stenting as a result of suboptimal gastric decompression from the NG tube. Primary and secondary outcomes are summarized in Table 2. Technical success was achieved in 16 patients. The two patients in whom stent placements was unsuccessful underwent successful palliative surgical gastrojejunostomy procedures. Seven patients had concurrent metallic biliary stents and one patient had undergone previous Roux-en-Y-hepaticojejunostomy for benign common bile duct (CBD) stricture. In two patients, there was no documented poststenting oral intake, although in both patients data on LOS and OS were available: one patient was a tertiary referral and was not followed up by our institute after discharge, and the other patient was transferred to the local hospice after the procedure for end-of-life care and was not followed up clinically. In the remaining 14 patients, the mean gastric outlet obstruction scoring system score improved from 0.63 (preprocedure) to 2.57 (postprocedure), which represents a statistically significant difference (P < 0.0001). There was only one periprocedural complication. The patient had a metallic biliary stent in situ and developed cholangitis a week after duodenal stent implantation. No biliary obstruction was found on ultrasonography, and the patient was treated with antibiotics and made a full recovery. Four patients died within 30 days of the procedure, although none of the deaths were procedure related. Two patients died during the same episode of admission, 13 and 24 days post procedure respectively. Both had shown symptomatic improvement. The median LOS for the 16 patients who successfully underwent SEMS insertion was 4 days, and the median OS was 58 days (Fig. 2). Radiological imaging follow-up was conducted in 12 patients, with a median time of 44 days (Fig. 3). Fourteen patients were clinically followed up until death, with two patients still alive at the time of this report. One reintervention was performed after 160 days in a patient who had recurrent symptoms from tumour overgrowth of the stent; this patient underwent a successful second SEMS insertion (stent in stent) and survived for another 73 days. Discussion

The aim of gastroduodenal stenting is to re-establish luminal patency, thus allowing enteral feeding in patients with obstructive symptoms and improvement in the quality of life [20]. Although various randomized controlled trials have produced conflicting conclusions, it is generally accepted that patients who undergo SEMS insertion have comparable complication rates and OS to gastrojejunostomy patients, but with the added benefit of tolerating oral intake more rapidly post procedure and with a much shorter LOS [7,21–23]. Duodenal stents are available as covered or uncovered (bare-metal) stents and are used under different circumstances. Bare-metal stents are more prone to tumour ingrowth and may require reintervention; however, they have a lower risk of stent migration, a longer median patency rate and allow concurrent stenting for biliary obstruction, commonly seen in patients with pancreatic or biliary tree malignancies [24–28].

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Fig. 1. Steps of SEMS deployment. (a) A wide-bore NG tube is inserted into the patient’s stomach at least 24 h before the procedure to decompress the stomach. (b) A front-viewing gastroscope is used and advanced as far as possible into the duodenum. Water-soluble contrast is then used to identify and assess the stricture. (c) After the stricture is recannulized with a catheter and a hydrophilic guidewire, a stiff guidewire is placed across the stricture with the tip at least 10 cm distal to the stricture. (d) The SEMS is deployed across the stricture using an ‘over-the-scope’ technique. Satisfactory deployment is confirmed with water-soluble contrast and by direct visualization. SEMS, self-expandable metal stents.

Previous studies related to duodenal stenting have concentrated on proximal duodenal obstruction and have demonstrated high technical and clinical success rates, as well as low morbidity and mortality. The technical success rates in most of these studies are over 90%, with Jeurnink and colleagues showing a 96% success rate in their systematic review [16,24,29,30]. The clinical success rate is generally lower, ranging from 79–94%, depending on definition [19,30–33]. Distal duodenal stent placement has not been reported widely in the literature and is often

considered technically more challenging, with authors citing reasons such as endoscopically long distance to distal duodenal stenoses, loop formation of endoscopes in the stomach as well as the tortuous anatomy of the duodenum [19]. Despite these technical challenges, our technical success rate in this study is comparable to other published data on unselected duodenal obstructions (proximal and distal). Different strategies have previously been used to overcome the hurdles of stenting beyond the duodenal bulb. As

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Table 1. Patient characteristics Median age (years) Sex (M/F) Site of obstruction D2 D3 D4 Underlying malignancy Pancreatic carcinoma Gastric carcinoma Bile duct cancer Gallbladder cancer Duodenal cancer Others Previous biliary drainage Median time interval to intervention from initial diagnosis (days) Chemotherapy after procedure Median preprocedure radiological imaging (days)

70 (46–85) 8/10 12 4 2 9 3 1 1 1 3 7 238 (12–2933) 6/16 5 (0–13)

Table 2. Outcome of patients who underwent SEMS for obstruction beyond the duodenal bulb Technical success Clinical success GOSS score Mean prestenting score Mean poststenting score Periprocedural complications 30-day mortality Reintervention Median length of hospital stay post procedure (days) Median follow-up radiological imaging (days) Median overall survival (days)

16/18 13/14

Fig. 3. Follow-up radiological images were available in 12 patients. Many 0.63 2.57 (P < 0.0001) 1/16 4/16 1/14 4 (0–19)a 44 (3–310)b 58 (14–394)a

Two patients were lost to follow-up in this cohort. SEMS, self-expandable metal stents. a Results collected from all 16 patients who underwent SEMS insertion successfully. b Data collected from 14 patients in whom clinical follow-up data were available.

Survival function

Cumulative survival

1.0

Median survival = 67 days

0.8 All malignancies Pancreatic cancer

0.6 0.4 0.6 0.0 0

100

200 Time / days

300

400

Fig. 2. Overall survival of the 16 patients who underwent SEMS insertion successfully for obstruction beyond the duodenal bulb. The overall survival is similar between patients suffering from pancreatic cancer and those with other cancers. SEMS, self-expandable metal stents.

conventional front-viewing gastroscopes may not be long enough to reach the distal duodenal obstruction, Jeurnink et al. [34] used colonoscopes in 16 patients, with a technical success rate of 93%. Similarly, Park et al. [35] used side-viewing duodenoscopes in 31 patients, with a technical success rate of 87%. In an attempt to provide more stability to positioning and stent deployment, Espinel and Pinedo [36] published a case report on the use of an

underwent CT scanning to assess their response to cancer treatment. This is a coronal CT image of the abdomen that shows the duodenal stent to be fully patent. CT, computed tomography.

enteroscopy overtube as an adjunct with a single-balloon enteroscope for obstruction at the angle of Treitz. Otherwise, guiding sheaths have also been advocated by Park et al. [37] to avoid guidewire looping in the proximal bowel from affecting stent deployment, and they have achieved a technical success rate of 98% in 72 patients with duodenal obstruction beyond the first part of the duodenum. Several authors have advocated gastroduodenal stenting through a percutaneous transgastric approach, with Miller’s team deploying 35 stents for duodenal obstruction with a 90% success rate, although the number of distal duodenal obstructions was not identified in their study [38]. New types of stents have also been introduced to overcome the tortuous anatomy while maintaining enough radial force and flexibility. Zhou et al. [30] successfully deployed six newly designed braided nitinol stents in a nested configuration using a low profile 10 F delivery system under fluoroscopic guidance alone. Our experience shows that stenting beyond the duodenal bulb is technically feasible and safe using standard front-viewing gastroscopes and does not necessarily require specialist equipment. In our study, all cases were discussed in a multidisciplinary meeting at our hospital and a standardized pathway was followed. The same type of gastroscope and stent were used in each case regardless of the length or location of the obstruction. Although prescriptive, these steps ensured that the operators performing these procedures were familiar with the equipment and procedural steps, and the gastroscopes and stents were readily available at short notice. The rationale behind using bare-metal rather than covered stents was to allow normal biliary drainage in patients in whom the duodenal obstruction was close to or involving the ampulla of Vater but with no signs of biliary obstruction (six of 12 patients with D2 obstruction did not have biliary obstruction at presentation). Furthermore, placement of bare-metal stents

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Fig. 4. Water-soluble contrast study before the procedure to assess the duodenal obstruction. In this patient, a moderate stricture can be seen in the second part of the duodenum (grey arrows). This patient had undergone metallic biliary stent insertion previously because of concurrent biliary obstruction (black arrows).

Fig. 5. Axial CT image of the upper abdomen. The gallbladder cancer (black

does not preclude further biliary stenting through a percutaneous transhepatic approach should biliary obstruction subsequently develop. As for the length of the stent, 12 cm was chosen, as there is considerable shortening of the stent in the duodenum (>25%) after deployment. Little is known about the length of duodenal obstruction in this cohort, although in our experience long strictures are not common. We found that this length was suitable in all our cases, and no overlapping stenting was required. As in all procedures, adequate preprocedural planning and patient preparation are key to success. All our patients had NG tube preparation as per international guidelines and underwent preprocedural radiological imaging to demonstrate the degree and location of the obstruction (Figs 4 and 5). The most common reasons cited for technical failure are inability of the guidewire to traverse the stricture, inability of the stent delivery system to reach the lesion, failure of stent deployment and early migration of the stent during the procedure [24,30,39]. Indeed, in one of our failed cases, we were unable to traverse the stricture. In the other case, although we were able to cross the stricture, during the exchange of guidewires from a hydrophilic wire to a stiff wire in preparation for stent deployment, the wire slipped back and the position was lost, and the patient, thereafter, could not tolerate the procedure further. We believe that this is part of our learning curve, as these two cases were the first two attempts at our institute, and since then, the operators have improved on patient selection and technique, and no further technical failures have been recorded. The clinical success rate was high, and the immediate complication rate was low in our cohort. There was one patient in whom technical success was achieved but objective improvement in the gastric outlet obstruction scoring system score was not observed. He suffered from

pancreatic cancer and had duodenal obstruction at the D3 level. The reason for clinical failure was uncertain, as postprocedure water-soluble contrast study in the patient demonstrated the stent to have been patent and correctly deployed across the stricture. The patient survived for 46 days after the procedure. Another patient who had pancreatic head adenocarcinoma and obstruction at the D2 level developed cholangitis a week after the duodenal stenting. The patient already had a metallic biliary stent in situ, and cholangitis was thought to be secondary to a blocked biliary stent, although radiologically the biliary stent appeared to be patent, and ultrasonography did not show any evidence of biliary blockage. The patient was treated with intravenous antibiotics and settled without the need for any intervention. Our reintervention rate was also low, with only one patient requiring a further stent insertion because of tumour overgrowth 160 days after the initial stent deployment. There has been no meta-analysis or systematic review for purely distal duodenal obstruction as yet. In the metaanalysis by Nagaraja et al. [7], which included proximal duodenal obstruction, the mean OS for gastroduodenal stenting was 96 days, and in the study by No et al. [40], which was purely on gastric cancer and included all sites of obstruction, the median OS was as high as 189 days. Although our cohort had a much shorter OS, published survival data were mainly related to proximal duodenal obstruction, which is associated with a higher proportion of gastric and duodenal carcinomas, as compared with our cohort, in which over half of the patients suffered from pancreatic cancer. We believe that the results cannot be compared directly, as these are two distinct groups of patients and as patients with duodenal obstruction from pancreatic carcinoma are expected to have a shorter survival [24,41].

arrow) causes obstruction to the second part of the duodenum (grey arrow). The stomach and the first part of the duodenum is grossly dilated (white arrow). The patient had also undergone metallic biliary stent insertion previously for concurrent biliary obstruction (open arrow). CT, computed tomography.

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SEMS placement for malignant GDO Chiu et al.

Limitations of our study include the GOSS scores being applied retrospectively and the possibility of the results being influenced by observer bias. Similarly, the loss to follow-up of two patients in our small cohort may also contribute to attrition bias. We did not examine the overall LOS, but rather the postprocedural LOS. The reason for not examining the overall LOS in the hospital was that, as a tertiary centre, many patients were from other referring hospitals, and possible delays in referral and transfer do not reflect or relate to the clinical outcome of the patient [42]. Unfortunately, because of the retrospective nature of this study, we were unable to confidently identify time to oral intake tolerance. However, all our patients were instructed to start on clear oral fluids within 2 h and on a soft diet within 24 h of the procedure.

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Conclusion

Palliative stenting is a safe and clinically effective way to relieve malignant duodenal obstruction beyond the first part of the duodenum. This study has demonstrated that this can be done using conventional equipment and techniques. We believe that SEMS should be the treatment of choice because of its high technical and clinical success rates, as well as its low morbidity and complication rates in comparison with surgical gastrojejunostomies.

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Acknowledgements

We would like to thank Dr. James Cast and Dr. Oliver Byass, Hull and East Yorkshire Hospitals NHS Trust, as well as Dr. Prashanth Kumar, Doncaster and Bassetlaw Hospitals NHS Foundation Trust, for assisting in several of the cases. Conflicts of interest

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Self-expandable metal stent placement for malignant duodenal obstruction distal to the bulb.

Self-expandable metal stents (SEMS) are widely used for the palliative management of malignant proximal gastroduodenal obstruction because of its low ...
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