Diseases of the Esophagus (2014) ••, ••–•• DOI: 10.1111/dote.12260
Original article
Fully versus partially covered self-expandable metal stents in benign esophageal strictures A. Gangloff,1 S. Lecleire,1 A. Di Fiore,1 E. Huet,2 I. Iwanicki-Caron,1 M. Antonietti,1 P. Michel1 Departments of 1Gastroenterology and 2Digestive Surgery, Rouen University Hospital, Rouen, France
SUMMARY. Self-expandable plastic stents are currently recommended for refractory benign esophageal strictures but they show disappointing results in terms of migration and long-term efficacy. We report here our experience in the management of benign esophageal strictures with partially covered (PCSEMS) and fully covered self-expandable metal stents (FCSEMS). We performed a retrospective analysis of self-expandable metal stent (SEMS) placements for benign esophageal strictures from 1998 to 2011 in Rouen University Hospital. Twenty-two patients (15 men, 7 women) attempted 40 esophageal SEMS placements (17 PCSEMS, 23 FCSEMS) during this period. All technical complications were migrations. Migration was noted after 3/17 PCSEMS (17.6%) and 4/23 FCSEMS placement (17.4%, P = ns). Clinical complications occurred after 6/17 PCSEMS and 2/23 FCSEMS placements (35.3% vs. 8.7%, P = 0.053). PCSEMS caused two major complications (fistulae) whereas FCSEMS did not cause any major complication (11.7% vs. 0%). Mean dysphagia score was significantly lower after SEMS placement (1.68 vs. 3.08, P < 0.001) with similar results for PCSEMS and FCSEMS. Stent placement resulted in long-term clinical success for 23.5% of PCSEMS and 34.7% of FCSEMS (P = 0.0505). FCSEMS provide satisfying clinical success rate with an acceptable complication rate and they could constitute a relevant therapeutic option in the management of benign esophageal strictures. KEY WORDS: benign esophageal stricture, endoscopy, fully covered self-expandable metal stent, partially covered self-expandable metal stent.
INTRODUCTION Benign esophageal strictures can be caused by a variety of different etiologies, including reflux disease, caustic ingestion, surgery, or radiotherapy.1 They have a negative impact on the quality of life, mainly because of dysphagia and may even lead to lifethreatening complications such as aspiration or malnutrition. To date, endoscopic dilation using bougienage or balloons is the first intention treatment for such lesions.2 It usually results in symptom relief, but almost 40% of these strictures will recur during patient follow-up and 10% of patients remain refractory to endoscopic dilation.3,4 The successful use of partially covered selfexpandable metal stents (PCSEMS) in the palliation Address correspondence to: Dr Alice Gangloff, MD, Department of Gastroenterology, Rouen University Hospital, 1 rue de Germont, 76000 Rouen, France. Email: [email protected] © 2014 International Society for Diseases of the Esophagus
of malignant strictures led to evaluate these stents in benign strictures remaining refractory to endoscopic dilation.2,5,6 In former series, the use of PCSEMS in patients with benign strictures was associated with some major complications, including frequent hyperplastic tissue reaction resulting in the embedding of the stent in the esophageal wall leading to obstruction, perforation, or impossible removal.7–9 These complications led to the development of selfexpandable plastic stents (SEPS), which were thought to prevent this hyperplastic tissue reaction. Despite promising initial results, last series report frequent stent migration, few long-term symptom relief, and still some cases of hyperplastic tissue reaction.10–14 Fully covered self-expandable metal stents (FCSEMS) could represent an interesting alternative but to date, data are not sufficient for a definitive conclusion. We report in this series our experience in the management of benign esophageal strictures with self-expandable metal stent (SEMS) including PCSEMS and FCSEMS. 1
2
Diseases of the Esophagus
MATERIALS AND METHODS
35
Data collection
30
This is a retrospective case review of patients who underwent SEMS placement for benign esophageal strictures from 1998 to 2011 in Rouen University Hospital. No Institutional Review Board was solicited. Patient selection was performed in the electronic medical record using the code for ‘esophageal stenting’. Chart review provided retrospective information including age and sex of the patients, etiology, location and length of the stricture, number of previous dilations, stent type, technical and clinical complications, and clinical outcome. Indications for stent placement were categorized into three groups: (i) benign esophageal disease including reflux disease and caustic lesions; (ii) radiation-induced and post-photodynamic therapy (PDT) strictures; and (iii) anastomotic strictures. Technical success was defined as the correct placement of the stent within the stricture and technical complication corresponded to migration or reintervention. Dysphagia severity was retrospectively graded using patient charts according to the Ogilvie et al. classification:15 grade 0, ability to eat a normal diet; grade 1, ability to eat some solid food; grade 2, ability to eat some semisolids only; grade 3, ability to swallow liquids only; and grade 4, complete dysphagia. Short-term clinical success corresponded to regression of the dysphagia (i.e. improvement of the dysphagia score) during the first month after stenting. Final clinical outcome was defined as clinical outcome at the end of the follow-up. It was categorized into final clinical success and final clinical failure. Final clinical success was defined as dysphagia remission without the need for dilation, stent placement, or surgery after stenting at the end of the follow-up. Hyperplastic tissue reactions at the proximal end of the stent leading to recurrent obstructions were considered as clinical failure as well as stricture recurrence occurring after stent removal or after stent migration. Minor complications included pain and resolutive food impactions. Major complications included aspiration, perforation or fistula, and hemorrhage.
25
Statistical analysis Results were expressed as percentages or means for continuous variables. Time to migration, time to clinical failure (i.e. hyperplastic obstruction of the stent or stricture recurrence), and follow-up were expressed in median days. Fisher’s exact test was used to compare continuous data, as appropriate. RESULTS Twenty-two patients (15 men, 7 women) with a mean age of 67 years (range: 45–87) attempted at least one
20 FCSEMS
15
PCSEMS
10 5 0 1998–2004
2005–2011
Fig. 1 Type of self-expandable metal stent (SEMS) evolution from 1998 to 2011. FCSEMS, fully covered self-expandable metal stent; PCSEMS, partially covered self-expandable metal stent.
esophageal SEMS placement for benign esophageal stricture from 1998 to 2011 in Rouen University Hospital. The etiology of the stricture was reflux disease for eight patients (36%), PDT for one patient (4.5%), radiotherapy for six patients (27%), anastomotic stricture for five patients (23%), and radiotherapy associated with anastomotic stricture for two patients (9%). The stricture was located to the upper esophagus for seven patients (31.8%), to the mid-esophagus for seven patients (31.8%), and to the lower esophagus for eight patients (36.4%). The mean length of the stricture was 3 cm (range: 1–6.5 cm) and the mean dilation number before stenting was 2.9 with an average time of 79 days (range: 7–518) between two dilations. For one patient, the esophageal stricture was associated with an anastomotic leak. All patients received general anesthesia for stent placement. From 1998 to 2011, 40 SEMS were placed in 22 patients. To allow passage of the endoscope through the stricture, esophageal dilation was performed before stenting for 32 of 40 (80%) procedures (26 bougienage dilations, 6 balloon dilations). Seventeen of 40 SEMS (42.5%) were PCSEMS. All of them were partially covered Ultraflex® stents (Microvasive/Boston Scientific Corp, Natick, MA, USA). Twenty-three of 40 SEMS (57.5%) were FCSEMS. The repartition of FCSEMS was as follows: (i) 12 Choostent® SEMS (M.I.Tech, Seoul, Korea); (ii) 8 Hanarostent® SEMS (Life Partners Europe, Bagnolet, France); (iii) 1 Wallflex® SEMS (Microvasive/Boston Scientific Corp); and (iv) 2 totally covered Taewong® SEMS (Taewong Medical, Gyeonggi do, South Korea). During the period 2006– 2011, FCSEMS were more frequently used as compared with the period 1998–2005 (74% vs. 0% P < 0.001, Fig. 1). In the same period (1998–2011), only one SEPS was placed for benign esophageal stricture. Stent placement was successful in 100% of SEMS placement attempts. Technical data and clinical outcome after stent placement are resumed in a flow chart (Fig. 2). © 2014 International Society for Diseases of the Esophagus
SEMS in benign esophageal strictures
3
40 SEMS 17 PCSEMS
Migration n=3
23 FCSEMS
Migration n=4
Fistulae n=2
Planned extraction n=9
No extraction n = 10
Stricture recurrence n=3
Hyperplastic obstruction n=8
Cancer recurrence n=1
Hyperplastic obstruction n=8
Oesophageal motor troubles n=1 Success n=2 Final clinical success n = 4 (23.5%) Median Follow-Up: 90 days (20–405)
Success n=4
Success n=2
Final clinical success n = 8 (34.7%) Median Follow-Up: 208 days (13–744)
Fig. 2 Flow chart for partially covered self-expandable metal stents (PCSEMS) and fully covered self-expandable metal stents (FCSEMS).
All technical complications were migrations. Migration was noted after 3 of 17 PCSEMS (17.6%) and after 4 of 23 FCSEMS placement (17.4%, P = ns, Fig. 2). Three of 23 FCSEMS had been fixed with clips at the proximal end of the stent to prevent their migration but one migration occurred despite clip fixation. The median time to migration was 37 days, without any significant difference between PCSEMS and FCSEMS. Migration occurred for 4 of the 22 SEMS (18.2%) placed in the lower esophagus, for 1 of the 6 SEMS (16.7%) placed in the mid-esophagus, and in 2 of the 12 SEMS (16.7%) placed in the upper esophagus (P = ns). Migration rates were also analyzed by indication, with rates of 33%, 0%, 30%, and 10% for peptic, post-radiotherapy, anastomotic, and hyperplastic strictures, respectively (P = ns). Clinical complications occurred after 6 of 17 PCSEMS placement and after 2 of 23 FCSEMS placements (35.3% vs. 8.7%, P = 0.053) (Table 1). PCSEMS caused two major complications corresponding to fistulae whereas FCSEMS did not cause any major complication (11.7% vs. 0%, P = 0.17). Both patients who developed fistula had received prior chemoradiotherapy in a curative intent for an esophageal cancer. Patient 1 was a middle-aged woman © 2014 International Society for Diseases of the Esophagus
treated in 1997 by Lewis-Santy esophagectomy for an esophageal adenocarcinoma and then in 2001 with chemoradiotherapy for a local recurrence. Esophageal stricture occurred in 2004 without evident cancer recurrence. Indeed, computed tomography (CT) scan and gastroscopy did not show any esophageal lesion and iterative biopsies remained negative. PCSEMS was inserted in April 2004 and eso-tracheal fistula was revealed in October 2004 by a severe aspiration pneumonia. At this time, gastroscopy showed eso-tracheal fistula facing an embedding of the proximal end of the stent. Esophageal biopsies remained negative. Double
Table 1 Complications after fully covered self-expandable stent (FCSEMS) placement in comparison with partially covered selfexpandable stent (PCSEMS) placement
Major complications Fistulae Minor complications Food impaction Pain Total
FCSEMS (n = 23)
PCSEMS (n = 17)
0 (0%) 0 2 (8.7%) 1 1 2 (8.7%)
2 (11.8%) 2 4 (23.5%) 4 0 6 (35.3%)
P = 0.17 P = 0.37 P = 0.053
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Diseases of the Esophagus
stenting of esophagus and airway was performed but clinical evolution was unfavorable and led to the death of the patient in January 2005. Patient 2 was a 78-years-old man treated in 2008 with definitive chemoradiotherapy for an esophageal epidermoid carcinoma. Two months later, he developed an esophageal stricture. Surgery was ruled out because of age and iterative biopsies remained negative. A FCSEMS was inserted in December 2008 but a hyperplastic granulation tissue became symptomatic in January 2009 and led to the insertion of a PCSEMS at the proximal end of the first stent. Eso-tracheal fistula occurred in June 2009 and was managed with double stenting of esophagus and airway and endoscopic gastrostomy for enteral nutrition. Unfortunately, clinical evolution was unfavorable and led to the death of the patient in January 2010. Short-term clinical efficacy was assessable for 25 of 40 stent placements. Twenty-three of 25 (92%) SEMS resulted in symptomatic improvement and two of 25 (8%) stents resulted in stable dysphagia. No dysphagia aggravation occurred after stent placement. Mean dysphagia score was significantly lower after SEMS placement (1.68 vs. 3.08, P < 0.001) with similar results for PCSEMS (1.71 vs. 2.93, P < 0.001) and for FCSEMS (1.64 vs. 3.23, P = 0.0004). Stent placement resulted in final clinical success in 23.5% and 34.7% respectively for PCSEMS and FCSEMS (P = 0.0505, Fig. 2). The median follow-up for clinical success was 90 days (range: 20–405) for PCSEMS and 208 days (range: 13–744) for FCSEMS. In the subgroup of PCSEMS, no stent had a planned extraction. The causes of clinical failure in this group were: migration resulting in stricture recurrence for 3 of 17 stents (17.6%), secondary fistula for 2 of 17 stents (11.8%), and hyperplastic obstruction at the proximal end of the stent for 8 of 17 stents (47%). The median time to hyperplastic obstruction was 128 days (range: 28–425) (Fig. 2). In the subgroup of FCSEMS, 4 of 23 (17.4%) presented migration after a median time of 45 days (range: 12–143), 9 of 23 stents (39.1%) were removed after a median time of 34 days (range: 15–79), and 10 of 23 (43.5%) remained in place. Stent removal resulted in clinical success for four of nine (44.4%) stents with a median follow-up of 208 days (28–744). Causes of failure were: (i) cancer recurrence for one patient (11.1%); (ii) persistent dysphagia due to esophageal motor troubles for one patient (11.1%%); and (iii) stricture recurrence for three patients (60%). The median time to stricture recurrence after stent removal was 107 days (90–122). After migration, clinical success occurred in two of four cases (follow-up: 329 days) and stricture recurrence occurred in two of four cases. The median time to stricture recurrence was 113 days (range: 56–169).
Ten stents remained in place. Only two of them (20%) resulted in clinical success. The cause of clinical failure was recurrent stricture at the proximal end of the stent for these eight stents after a median time of 112 days (range: 37–356). Finally, we analyzed final clinical outcome according to the type of stricture using the three pre-defined groups of indications, regardless of the type of SEMS. Final clinical success rate was 20% for radiation induced and post-PDT strictures, 45% for anastomotic strictures, and 26% for peptic strictures but differences did not reach statistical significance threshold (P = 0.44).
DISCUSSION In this study, we report our experience over more than one decade in the management of benign esophageal strictures with SEMS. Most of the strictures were complex strictures as defined by Lew and Kochman in 2002.16 Indeed, the mean stricture length was 3 cm and 80% of SEMS placement required prior dilation to allow the passage of the endoscope through the stricture. We confirm here the high technical success rate and the short-term clinical efficacy associated with FCSEMS and PCSEMS. Nevertheless, our main results concern final outcome and complication rates, which are known to be disappointing for SEPS.13,14 We report 34.7% of final clinical success for FCSEMS with a median follow-up of 208 days versus 23.5% of final clinical success with a median follow-up of 90 days for PCSEMS (P = 0.0505). Clinical success rate even reaches 46.1% in the subgroup of temporary FCSEMS (i.e. after stent migration or removal). Although we do not reach statistical difference between PCSEMS and FCSEMS, comparison of these results with previous data supports the use of FCSEMS placement in this indication. To date, few authors reported their experience in the FCSEMS management for benign esophageal strictures. In 2010, Eloubeidi et al. reported a series of 19 temporary FCSEMS placed in benign esophageal strictures. The same year, Bakken et al. published the largest series of FCSEMS with 107 FCSEMS insertions including only 40 for benign esophageal stricture. With a total of 23 FCSEMS placements, our series represents the second largest series of FCSEMS placed in benign esophageal strictures. Although comparison is made difficult because stent extraction was not routinely performed in our series, our results seem to be slightly better as compared with these two previous studies. Indeed, Eloubeidi and Lopes reported 21% of clinical success.17 In the study published by Bakken et al., long-term follow-up was defined as more than 4 months after stent removal.18 Clinical improvement at stent removal was present © 2014 International Society for Diseases of the Esophagus
SEMS in benign esophageal strictures
for 14 of 25 patients (60%) but long-term clinical success was assessable only for six patients and it only occurred for two of six patients (33%). Data concerning SEPS are heterogeneous. The first two studies published reported a clinical efficacy of 81% and 80% respectively with a median follow-up longer than 20 months.10,11 The two others reported disappointing results with only 5 of 83 procedures (6%) leading to long-term symptom relief.13 We also confirm with this study that FCSEMS tend to cause less complications and particularly less major complications than PCSEMS. Indeed, we report minor complications after 2 of 23 FCSEMS (8.7%) versus 4 of 17 PCSEMS (23.5%, P = 0.37) and major complication after 0 of 23 FCSEMS (0%) versus 2 of 17 PCSEMS (11.8%, P = 0.17). Global complication rates are 8.7% for FCSEMS versus 35.3% for PCSEMS (P = 0.053). Although these results do not reach statistical significance, they are clinically relevant and they are in agreement with previous studies. Indeed, as regard FCSEMS, Eloubeidi et al. only reported one major complication (arrhythmia) in 19 patients (5.2%) and Bakken et al. only two major immediate complications (stridor) in 40 procedures (5%).17,18 Concerning PCSEMS, fistulae occurrence after stent placement have already been described.8 We report here two fistulae after PCSEMS placement. Both concerned patients previously treated with chemoradiotherapy for an esophageal cancer. Although the doubt remains concerning cancer remission owing to a short follow-up and the absence of surgery, we considered these patients to be in clinical complete response in so far as iterative esophageal biopsies and CT scan remained negative. Our series does not allow us to conclude concerning the risk of fistula associated with PCSEMS. Indeed the cause of the stricture and prior treatments such as chemoradiotherapy could also be associated with fistula, as already suggested by our team. Nevertheless, these two cases suggest us to be cautious with the use of PCSEMS in benign esophageal strictures. Surprisingly, we do not show in this study any significant difference in terms of migration between PCSEMS and FCSEMS (17.6% vs. 17.4%, P = ns). Indeed, our migration rate in FCSEMS is low in comparison with Eloubeidi et al. who reported seven migrations in 19 patients (37%) and Bakken et al. who reported migration rates of 50%, 25%, and 60% for benign refractory, radiation, and anastomotic strictures, respectively.17,18 The fixation of the proximal end of the stent with clips in 3 of 23 procedures is not sufficient to explain our low rate of migration with FCSEMS because it does not prevent migration. Indeed migration occurred after one of three clip fixations. Besides, comparison with SEPS is difficult because of the heterogeneity of the studies, which report migration rates varying between 24% and 63.9%.10,13,14 © 2014 International Society for Diseases of the Esophagus
5
The high rate of PCSEMS used for benign stricture in our institution from 1998 to 2004 could appear surprising. Indeed, as previously reported, publications have shown since 1999 that the use of SEMS was associated with major complications such as ingrowths of granulation tissue at the proximal end of the stent leading to stricture recurrence, perforation, or removal difficulties.8,9,19 Nevertheless, most of these publications were case reports or included a small number of patients, leading many operators to look for their own experience. Our series of 17 PCSEMS placement in benign esophageal strictures confirms most of previously reported data. Indeed, we confirm in this series the short-term clinical efficacy of PCSEMS attested by a significant decrease in dysphagia score after stent placement (1.71 vs. 2.93, P < 0.001). However, this optimistic result should be balanced by the high risk of complication (35.3% including 11.8% of major complications) and the poor final clinical success rate (23.5% with a median follow-up of 90 days). It must be noticed that no PCSEMS had a planned extraction in this study. This attitude probably had two main explanations. First, operators were trained in handling PCSEMS in malignant esophageal stricture and they first applied, probably detrimentally, the same rules to benign strictures. Secondly, none of our patients underwent surgery, probably because of age and comorbidities and operators probably wanted to avoid multiples interventions, leaving these stents permanently. This attitude with PCSEMS could partly explain the low rate of clinical success by increasing the risk of hyperplastic tissue reaction at the proximal end of the mesh and consequently the high rate of fistulae. Interestingly, in this series, the median time to hyperplastic obstruction was 128 days (28–425). This result suggests that early removal could prevent most of hyperplastic tissue reactions and allow the use of temporary PCSEMS in benign esophageal strictures. Siersema has previously proposed this attitude in 2008.2 SEPS were developed to minimize the risk of hyperplastic reaction and were recommended until recently in benign esophageal strictures.2 In our institution, the use since 2004 of FCSEMS instead of SEPS had practical reasons: (i) operators were trained in handling SEMS because of their experience in malignant esophageal stricture management; (ii) SEPS applicators are stiff and large compared with applicators used for SEMS; and (iii) SEPS are more expensive than SEMS. Nevertheless, some recent studies report for SEPS frequent migrations and a lack of clinical efficacy in the treatment of benign esophageal strictures.13,14 These disappointing results led us to report our series of FCSEMS to assess the place of FCSEMS, and our results support the use of SEMS in the management of benign esophageal strictures.
6
Diseases of the Esophagus
The present study suggests that PCSEMS as FCSEMS can be complicated by tissue ingrowth leading to embedding of the stent in the esophageal wall, as initially reported by Jaganmohan and Raju in 2008.20 We report here 80% of hyperplastic tissue granulation leading to recurrent obstruction after a median time of 112 days when FCSEMS remain in place. This rate appears to be very high in comparison with previous studies. Indeed, these studies should not be compared because almost all the stents were systematically removed in the previous studies. Bakken et al. reported 12 tissue granulations after 104 FCSEMS placements (11.5%) for benign esophageal disease (including strictures, fistulae/leaks, and perforations): seven were obstructive and five were mild. These hyperplastic reactions were described at the time of stent extraction after a mean duration of 88 days (range: 7–209), but they did not preclude stent extraction. In the series published by Eloubeidi et al., FCSEMS remained in place during 64 ± 74 days without any hyperplastic obstruction. These results underline the requirement of an early stent removal, probably 4 to 8 weeks after stent placement. In conclusion, FCSEMS provide satisfying clinical success rate with an acceptable complication rate in the management of benign esophageal strictures and they could constitute a relevant therapeutic option in this indication. Nevertheless, the use of FCSEMS does not preclude hyperplastic tissue reaction at the end of the stent, as previously reported for PCSEMS. Early removal should be systematically planned for FCSEMS to prevent complications. References 1 Spechler S J. American gastroenterological association medical statement on treatment of patients with dysphagia caused by benign disorders of the distal esophagus. Gastroenterology 1999; 117: 229–33. 2 Siersema P D. Treatment options for esophageal strictures. Nat Clin Pract Gastroenterol Hepatol 2008; 5: 142–52. 3 Pereira-Lima J C, Ramires R P, Zamin I Jr et al. Endoscopic dilation of benign esophageal strictures: report on 1043 procedures. Am J Gastroenterol 1999; 94: 1497–501. 4 Said A, Brust D J, Gaumnitz E A et al. Predictors of early recurrence of benign esophageal strictures. Am J Gastroenterol 2003; 98: 1252–6.
5 Siersema P D, Hop W C, Van Blankenstein M et al. A comparison of three types of covered metal stents for the palliation of patients with dysphagia caused by oesogastric carcinoma: a prospective, randomized study. Gastrointest Endosc 2001; 54: 145–53. 6 Conio M, Repici A, Battaglia G et al. A randomised prospective comparison of self-expandable plastic stents and partially covered self-expandable metal stents in the palliation of malignant esophageal dysphagia. Am J Gastroenterol 2007; 103: 2667–77. 7 Wadhwa R P, Kozarek R A. Use of self-expandable metallic stents in benign GI diseases. Gastrointest Endosc 2003; 58: 207–12. 8 Ackroyd R, Watson D I, Devitt P G et al. Expandable metallic stents should not be used in the treatment of benign esophageal strictures. J Gastroenterol Hepatol 2001; 16: 484–7. 9 Fiorini A, Fleischer D, Valero J et al. Self-expandable metal coil stents in the treatment of benign esophageal strictures refractory to conventional therapy: a case series. Gastrointest Endosc 2000; 52: 259–62. 10 Repici A, Conio M, De Angelis C et al. Temporary placement of an expandable polyester silicone-covered stent for treatment of refractory benign esophageal strictures. Gastrointest Endosc 2004; 60: 513–9. 11 Evrard S, Le Moine O, Lazaraki G et al. Self-expanding plastic stents for benign esophageal lesions. Gastrointest Endosc 2004; 60: 894–900. 12 Dua K S, Vleggar F P, Santharam R et al. Removable self-expanding plastic esophageal stent as a continuous, nonpermanent dilator in treating refractory benign esophageal strictures: a prospective two-center study. Am J Gastroenterol 2008; 103: 2988–94. 13 Holm A N, Baron T H. Self-expanding plastic stents in treatment of benign esophageal conditions. Gastrointest Endosc 2008; 67: 20–5. 14 Oh Y, Kochman M L, Ahmad N A, Ginsberg G G. Clinical outcomes after self-expanding plastic stent placement for refractory benign esophageal strictures. Dig Dis Sci 2010; 55: 1344–8. 15 Ogilvie A L, Dronfield M W, Ferguson R, Atkinson M. Palliative intubation of oesophagogastric neoplasms at fibreoptic endoscopy. Gut 1982; 23: 1060–7. 16 Lew R J, Kochman M L. A review of endoscopic methods of esophageal dilation. J Clin Gastroenterol 2002; 35: 117– 26. 17 Eloubeidi M A, Lopes T L. Novel removable internally fully covered self expanding metal esophageal stent: feasibility, technique of removal and tissue response in humans. Am J Gastroenterol 2009; 104: 1374–81. 18 Bakken J C, Wong Kee Song L M, de Groen P C, Baron T H. Use of a fully covered self-expandable metal stent for the treatment of benign esophageal diseases. Gastrointest Endosc 2010; 72: 712–20. 19 Sandha G S, Marcon N E. Expandable metal stents for benign esophageal obstruction. Gastrointest Endosc Clin N Am 1999; 9: 437–46. 20 Jaganmohan S, Raju G S. Tissue ingrowth in a fully covered self-expandable metallic stent (with videos). Gastrointest Endosc 2008; 68: 602–4.
© 2014 International Society for Diseases of the Esophagus
Original article
Fully versus partially covered self-expandable metal stents in benign esophageal strictures A. Gangloff,1 S. Lecleire,1 A. Di Fiore,1 E. Huet,2 I. Iwanicki-Caron,1 M. Antonietti,1 P. Michel1 Departments of 1Gastroenterology and 2Digestive Surgery, Rouen University Hospital, Rouen, France
SUMMARY. Self-expandable plastic stents are currently recommended for refractory benign esophageal strictures but they show disappointing results in terms of migration and long-term efficacy. We report here our experience in the management of benign esophageal strictures with partially covered (PCSEMS) and fully covered self-expandable metal stents (FCSEMS). We performed a retrospective analysis of self-expandable metal stent (SEMS) placements for benign esophageal strictures from 1998 to 2011 in Rouen University Hospital. Twenty-two patients (15 men, 7 women) attempted 40 esophageal SEMS placements (17 PCSEMS, 23 FCSEMS) during this period. All technical complications were migrations. Migration was noted after 3/17 PCSEMS (17.6%) and 4/23 FCSEMS placement (17.4%, P = ns). Clinical complications occurred after 6/17 PCSEMS and 2/23 FCSEMS placements (35.3% vs. 8.7%, P = 0.053). PCSEMS caused two major complications (fistulae) whereas FCSEMS did not cause any major complication (11.7% vs. 0%). Mean dysphagia score was significantly lower after SEMS placement (1.68 vs. 3.08, P < 0.001) with similar results for PCSEMS and FCSEMS. Stent placement resulted in long-term clinical success for 23.5% of PCSEMS and 34.7% of FCSEMS (P = 0.0505). FCSEMS provide satisfying clinical success rate with an acceptable complication rate and they could constitute a relevant therapeutic option in the management of benign esophageal strictures. KEY WORDS: benign esophageal stricture, endoscopy, fully covered self-expandable metal stent, partially covered self-expandable metal stent.
INTRODUCTION Benign esophageal strictures can be caused by a variety of different etiologies, including reflux disease, caustic ingestion, surgery, or radiotherapy.1 They have a negative impact on the quality of life, mainly because of dysphagia and may even lead to lifethreatening complications such as aspiration or malnutrition. To date, endoscopic dilation using bougienage or balloons is the first intention treatment for such lesions.2 It usually results in symptom relief, but almost 40% of these strictures will recur during patient follow-up and 10% of patients remain refractory to endoscopic dilation.3,4 The successful use of partially covered selfexpandable metal stents (PCSEMS) in the palliation Address correspondence to: Dr Alice Gangloff, MD, Department of Gastroenterology, Rouen University Hospital, 1 rue de Germont, 76000 Rouen, France. Email: [email protected] © 2014 International Society for Diseases of the Esophagus
of malignant strictures led to evaluate these stents in benign strictures remaining refractory to endoscopic dilation.2,5,6 In former series, the use of PCSEMS in patients with benign strictures was associated with some major complications, including frequent hyperplastic tissue reaction resulting in the embedding of the stent in the esophageal wall leading to obstruction, perforation, or impossible removal.7–9 These complications led to the development of selfexpandable plastic stents (SEPS), which were thought to prevent this hyperplastic tissue reaction. Despite promising initial results, last series report frequent stent migration, few long-term symptom relief, and still some cases of hyperplastic tissue reaction.10–14 Fully covered self-expandable metal stents (FCSEMS) could represent an interesting alternative but to date, data are not sufficient for a definitive conclusion. We report in this series our experience in the management of benign esophageal strictures with self-expandable metal stent (SEMS) including PCSEMS and FCSEMS. 1
2
Diseases of the Esophagus
MATERIALS AND METHODS
35
Data collection
30
This is a retrospective case review of patients who underwent SEMS placement for benign esophageal strictures from 1998 to 2011 in Rouen University Hospital. No Institutional Review Board was solicited. Patient selection was performed in the electronic medical record using the code for ‘esophageal stenting’. Chart review provided retrospective information including age and sex of the patients, etiology, location and length of the stricture, number of previous dilations, stent type, technical and clinical complications, and clinical outcome. Indications for stent placement were categorized into three groups: (i) benign esophageal disease including reflux disease and caustic lesions; (ii) radiation-induced and post-photodynamic therapy (PDT) strictures; and (iii) anastomotic strictures. Technical success was defined as the correct placement of the stent within the stricture and technical complication corresponded to migration or reintervention. Dysphagia severity was retrospectively graded using patient charts according to the Ogilvie et al. classification:15 grade 0, ability to eat a normal diet; grade 1, ability to eat some solid food; grade 2, ability to eat some semisolids only; grade 3, ability to swallow liquids only; and grade 4, complete dysphagia. Short-term clinical success corresponded to regression of the dysphagia (i.e. improvement of the dysphagia score) during the first month after stenting. Final clinical outcome was defined as clinical outcome at the end of the follow-up. It was categorized into final clinical success and final clinical failure. Final clinical success was defined as dysphagia remission without the need for dilation, stent placement, or surgery after stenting at the end of the follow-up. Hyperplastic tissue reactions at the proximal end of the stent leading to recurrent obstructions were considered as clinical failure as well as stricture recurrence occurring after stent removal or after stent migration. Minor complications included pain and resolutive food impactions. Major complications included aspiration, perforation or fistula, and hemorrhage.
25
Statistical analysis Results were expressed as percentages or means for continuous variables. Time to migration, time to clinical failure (i.e. hyperplastic obstruction of the stent or stricture recurrence), and follow-up were expressed in median days. Fisher’s exact test was used to compare continuous data, as appropriate. RESULTS Twenty-two patients (15 men, 7 women) with a mean age of 67 years (range: 45–87) attempted at least one
20 FCSEMS
15
PCSEMS
10 5 0 1998–2004
2005–2011
Fig. 1 Type of self-expandable metal stent (SEMS) evolution from 1998 to 2011. FCSEMS, fully covered self-expandable metal stent; PCSEMS, partially covered self-expandable metal stent.
esophageal SEMS placement for benign esophageal stricture from 1998 to 2011 in Rouen University Hospital. The etiology of the stricture was reflux disease for eight patients (36%), PDT for one patient (4.5%), radiotherapy for six patients (27%), anastomotic stricture for five patients (23%), and radiotherapy associated with anastomotic stricture for two patients (9%). The stricture was located to the upper esophagus for seven patients (31.8%), to the mid-esophagus for seven patients (31.8%), and to the lower esophagus for eight patients (36.4%). The mean length of the stricture was 3 cm (range: 1–6.5 cm) and the mean dilation number before stenting was 2.9 with an average time of 79 days (range: 7–518) between two dilations. For one patient, the esophageal stricture was associated with an anastomotic leak. All patients received general anesthesia for stent placement. From 1998 to 2011, 40 SEMS were placed in 22 patients. To allow passage of the endoscope through the stricture, esophageal dilation was performed before stenting for 32 of 40 (80%) procedures (26 bougienage dilations, 6 balloon dilations). Seventeen of 40 SEMS (42.5%) were PCSEMS. All of them were partially covered Ultraflex® stents (Microvasive/Boston Scientific Corp, Natick, MA, USA). Twenty-three of 40 SEMS (57.5%) were FCSEMS. The repartition of FCSEMS was as follows: (i) 12 Choostent® SEMS (M.I.Tech, Seoul, Korea); (ii) 8 Hanarostent® SEMS (Life Partners Europe, Bagnolet, France); (iii) 1 Wallflex® SEMS (Microvasive/Boston Scientific Corp); and (iv) 2 totally covered Taewong® SEMS (Taewong Medical, Gyeonggi do, South Korea). During the period 2006– 2011, FCSEMS were more frequently used as compared with the period 1998–2005 (74% vs. 0% P < 0.001, Fig. 1). In the same period (1998–2011), only one SEPS was placed for benign esophageal stricture. Stent placement was successful in 100% of SEMS placement attempts. Technical data and clinical outcome after stent placement are resumed in a flow chart (Fig. 2). © 2014 International Society for Diseases of the Esophagus
SEMS in benign esophageal strictures
3
40 SEMS 17 PCSEMS
Migration n=3
23 FCSEMS
Migration n=4
Fistulae n=2
Planned extraction n=9
No extraction n = 10
Stricture recurrence n=3
Hyperplastic obstruction n=8
Cancer recurrence n=1
Hyperplastic obstruction n=8
Oesophageal motor troubles n=1 Success n=2 Final clinical success n = 4 (23.5%) Median Follow-Up: 90 days (20–405)
Success n=4
Success n=2
Final clinical success n = 8 (34.7%) Median Follow-Up: 208 days (13–744)
Fig. 2 Flow chart for partially covered self-expandable metal stents (PCSEMS) and fully covered self-expandable metal stents (FCSEMS).
All technical complications were migrations. Migration was noted after 3 of 17 PCSEMS (17.6%) and after 4 of 23 FCSEMS placement (17.4%, P = ns, Fig. 2). Three of 23 FCSEMS had been fixed with clips at the proximal end of the stent to prevent their migration but one migration occurred despite clip fixation. The median time to migration was 37 days, without any significant difference between PCSEMS and FCSEMS. Migration occurred for 4 of the 22 SEMS (18.2%) placed in the lower esophagus, for 1 of the 6 SEMS (16.7%) placed in the mid-esophagus, and in 2 of the 12 SEMS (16.7%) placed in the upper esophagus (P = ns). Migration rates were also analyzed by indication, with rates of 33%, 0%, 30%, and 10% for peptic, post-radiotherapy, anastomotic, and hyperplastic strictures, respectively (P = ns). Clinical complications occurred after 6 of 17 PCSEMS placement and after 2 of 23 FCSEMS placements (35.3% vs. 8.7%, P = 0.053) (Table 1). PCSEMS caused two major complications corresponding to fistulae whereas FCSEMS did not cause any major complication (11.7% vs. 0%, P = 0.17). Both patients who developed fistula had received prior chemoradiotherapy in a curative intent for an esophageal cancer. Patient 1 was a middle-aged woman © 2014 International Society for Diseases of the Esophagus
treated in 1997 by Lewis-Santy esophagectomy for an esophageal adenocarcinoma and then in 2001 with chemoradiotherapy for a local recurrence. Esophageal stricture occurred in 2004 without evident cancer recurrence. Indeed, computed tomography (CT) scan and gastroscopy did not show any esophageal lesion and iterative biopsies remained negative. PCSEMS was inserted in April 2004 and eso-tracheal fistula was revealed in October 2004 by a severe aspiration pneumonia. At this time, gastroscopy showed eso-tracheal fistula facing an embedding of the proximal end of the stent. Esophageal biopsies remained negative. Double
Table 1 Complications after fully covered self-expandable stent (FCSEMS) placement in comparison with partially covered selfexpandable stent (PCSEMS) placement
Major complications Fistulae Minor complications Food impaction Pain Total
FCSEMS (n = 23)
PCSEMS (n = 17)
0 (0%) 0 2 (8.7%) 1 1 2 (8.7%)
2 (11.8%) 2 4 (23.5%) 4 0 6 (35.3%)
P = 0.17 P = 0.37 P = 0.053
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stenting of esophagus and airway was performed but clinical evolution was unfavorable and led to the death of the patient in January 2005. Patient 2 was a 78-years-old man treated in 2008 with definitive chemoradiotherapy for an esophageal epidermoid carcinoma. Two months later, he developed an esophageal stricture. Surgery was ruled out because of age and iterative biopsies remained negative. A FCSEMS was inserted in December 2008 but a hyperplastic granulation tissue became symptomatic in January 2009 and led to the insertion of a PCSEMS at the proximal end of the first stent. Eso-tracheal fistula occurred in June 2009 and was managed with double stenting of esophagus and airway and endoscopic gastrostomy for enteral nutrition. Unfortunately, clinical evolution was unfavorable and led to the death of the patient in January 2010. Short-term clinical efficacy was assessable for 25 of 40 stent placements. Twenty-three of 25 (92%) SEMS resulted in symptomatic improvement and two of 25 (8%) stents resulted in stable dysphagia. No dysphagia aggravation occurred after stent placement. Mean dysphagia score was significantly lower after SEMS placement (1.68 vs. 3.08, P < 0.001) with similar results for PCSEMS (1.71 vs. 2.93, P < 0.001) and for FCSEMS (1.64 vs. 3.23, P = 0.0004). Stent placement resulted in final clinical success in 23.5% and 34.7% respectively for PCSEMS and FCSEMS (P = 0.0505, Fig. 2). The median follow-up for clinical success was 90 days (range: 20–405) for PCSEMS and 208 days (range: 13–744) for FCSEMS. In the subgroup of PCSEMS, no stent had a planned extraction. The causes of clinical failure in this group were: migration resulting in stricture recurrence for 3 of 17 stents (17.6%), secondary fistula for 2 of 17 stents (11.8%), and hyperplastic obstruction at the proximal end of the stent for 8 of 17 stents (47%). The median time to hyperplastic obstruction was 128 days (range: 28–425) (Fig. 2). In the subgroup of FCSEMS, 4 of 23 (17.4%) presented migration after a median time of 45 days (range: 12–143), 9 of 23 stents (39.1%) were removed after a median time of 34 days (range: 15–79), and 10 of 23 (43.5%) remained in place. Stent removal resulted in clinical success for four of nine (44.4%) stents with a median follow-up of 208 days (28–744). Causes of failure were: (i) cancer recurrence for one patient (11.1%); (ii) persistent dysphagia due to esophageal motor troubles for one patient (11.1%%); and (iii) stricture recurrence for three patients (60%). The median time to stricture recurrence after stent removal was 107 days (90–122). After migration, clinical success occurred in two of four cases (follow-up: 329 days) and stricture recurrence occurred in two of four cases. The median time to stricture recurrence was 113 days (range: 56–169).
Ten stents remained in place. Only two of them (20%) resulted in clinical success. The cause of clinical failure was recurrent stricture at the proximal end of the stent for these eight stents after a median time of 112 days (range: 37–356). Finally, we analyzed final clinical outcome according to the type of stricture using the three pre-defined groups of indications, regardless of the type of SEMS. Final clinical success rate was 20% for radiation induced and post-PDT strictures, 45% for anastomotic strictures, and 26% for peptic strictures but differences did not reach statistical significance threshold (P = 0.44).
DISCUSSION In this study, we report our experience over more than one decade in the management of benign esophageal strictures with SEMS. Most of the strictures were complex strictures as defined by Lew and Kochman in 2002.16 Indeed, the mean stricture length was 3 cm and 80% of SEMS placement required prior dilation to allow the passage of the endoscope through the stricture. We confirm here the high technical success rate and the short-term clinical efficacy associated with FCSEMS and PCSEMS. Nevertheless, our main results concern final outcome and complication rates, which are known to be disappointing for SEPS.13,14 We report 34.7% of final clinical success for FCSEMS with a median follow-up of 208 days versus 23.5% of final clinical success with a median follow-up of 90 days for PCSEMS (P = 0.0505). Clinical success rate even reaches 46.1% in the subgroup of temporary FCSEMS (i.e. after stent migration or removal). Although we do not reach statistical difference between PCSEMS and FCSEMS, comparison of these results with previous data supports the use of FCSEMS placement in this indication. To date, few authors reported their experience in the FCSEMS management for benign esophageal strictures. In 2010, Eloubeidi et al. reported a series of 19 temporary FCSEMS placed in benign esophageal strictures. The same year, Bakken et al. published the largest series of FCSEMS with 107 FCSEMS insertions including only 40 for benign esophageal stricture. With a total of 23 FCSEMS placements, our series represents the second largest series of FCSEMS placed in benign esophageal strictures. Although comparison is made difficult because stent extraction was not routinely performed in our series, our results seem to be slightly better as compared with these two previous studies. Indeed, Eloubeidi and Lopes reported 21% of clinical success.17 In the study published by Bakken et al., long-term follow-up was defined as more than 4 months after stent removal.18 Clinical improvement at stent removal was present © 2014 International Society for Diseases of the Esophagus
SEMS in benign esophageal strictures
for 14 of 25 patients (60%) but long-term clinical success was assessable only for six patients and it only occurred for two of six patients (33%). Data concerning SEPS are heterogeneous. The first two studies published reported a clinical efficacy of 81% and 80% respectively with a median follow-up longer than 20 months.10,11 The two others reported disappointing results with only 5 of 83 procedures (6%) leading to long-term symptom relief.13 We also confirm with this study that FCSEMS tend to cause less complications and particularly less major complications than PCSEMS. Indeed, we report minor complications after 2 of 23 FCSEMS (8.7%) versus 4 of 17 PCSEMS (23.5%, P = 0.37) and major complication after 0 of 23 FCSEMS (0%) versus 2 of 17 PCSEMS (11.8%, P = 0.17). Global complication rates are 8.7% for FCSEMS versus 35.3% for PCSEMS (P = 0.053). Although these results do not reach statistical significance, they are clinically relevant and they are in agreement with previous studies. Indeed, as regard FCSEMS, Eloubeidi et al. only reported one major complication (arrhythmia) in 19 patients (5.2%) and Bakken et al. only two major immediate complications (stridor) in 40 procedures (5%).17,18 Concerning PCSEMS, fistulae occurrence after stent placement have already been described.8 We report here two fistulae after PCSEMS placement. Both concerned patients previously treated with chemoradiotherapy for an esophageal cancer. Although the doubt remains concerning cancer remission owing to a short follow-up and the absence of surgery, we considered these patients to be in clinical complete response in so far as iterative esophageal biopsies and CT scan remained negative. Our series does not allow us to conclude concerning the risk of fistula associated with PCSEMS. Indeed the cause of the stricture and prior treatments such as chemoradiotherapy could also be associated with fistula, as already suggested by our team. Nevertheless, these two cases suggest us to be cautious with the use of PCSEMS in benign esophageal strictures. Surprisingly, we do not show in this study any significant difference in terms of migration between PCSEMS and FCSEMS (17.6% vs. 17.4%, P = ns). Indeed, our migration rate in FCSEMS is low in comparison with Eloubeidi et al. who reported seven migrations in 19 patients (37%) and Bakken et al. who reported migration rates of 50%, 25%, and 60% for benign refractory, radiation, and anastomotic strictures, respectively.17,18 The fixation of the proximal end of the stent with clips in 3 of 23 procedures is not sufficient to explain our low rate of migration with FCSEMS because it does not prevent migration. Indeed migration occurred after one of three clip fixations. Besides, comparison with SEPS is difficult because of the heterogeneity of the studies, which report migration rates varying between 24% and 63.9%.10,13,14 © 2014 International Society for Diseases of the Esophagus
5
The high rate of PCSEMS used for benign stricture in our institution from 1998 to 2004 could appear surprising. Indeed, as previously reported, publications have shown since 1999 that the use of SEMS was associated with major complications such as ingrowths of granulation tissue at the proximal end of the stent leading to stricture recurrence, perforation, or removal difficulties.8,9,19 Nevertheless, most of these publications were case reports or included a small number of patients, leading many operators to look for their own experience. Our series of 17 PCSEMS placement in benign esophageal strictures confirms most of previously reported data. Indeed, we confirm in this series the short-term clinical efficacy of PCSEMS attested by a significant decrease in dysphagia score after stent placement (1.71 vs. 2.93, P < 0.001). However, this optimistic result should be balanced by the high risk of complication (35.3% including 11.8% of major complications) and the poor final clinical success rate (23.5% with a median follow-up of 90 days). It must be noticed that no PCSEMS had a planned extraction in this study. This attitude probably had two main explanations. First, operators were trained in handling PCSEMS in malignant esophageal stricture and they first applied, probably detrimentally, the same rules to benign strictures. Secondly, none of our patients underwent surgery, probably because of age and comorbidities and operators probably wanted to avoid multiples interventions, leaving these stents permanently. This attitude with PCSEMS could partly explain the low rate of clinical success by increasing the risk of hyperplastic tissue reaction at the proximal end of the mesh and consequently the high rate of fistulae. Interestingly, in this series, the median time to hyperplastic obstruction was 128 days (28–425). This result suggests that early removal could prevent most of hyperplastic tissue reactions and allow the use of temporary PCSEMS in benign esophageal strictures. Siersema has previously proposed this attitude in 2008.2 SEPS were developed to minimize the risk of hyperplastic reaction and were recommended until recently in benign esophageal strictures.2 In our institution, the use since 2004 of FCSEMS instead of SEPS had practical reasons: (i) operators were trained in handling SEMS because of their experience in malignant esophageal stricture management; (ii) SEPS applicators are stiff and large compared with applicators used for SEMS; and (iii) SEPS are more expensive than SEMS. Nevertheless, some recent studies report for SEPS frequent migrations and a lack of clinical efficacy in the treatment of benign esophageal strictures.13,14 These disappointing results led us to report our series of FCSEMS to assess the place of FCSEMS, and our results support the use of SEMS in the management of benign esophageal strictures.
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The present study suggests that PCSEMS as FCSEMS can be complicated by tissue ingrowth leading to embedding of the stent in the esophageal wall, as initially reported by Jaganmohan and Raju in 2008.20 We report here 80% of hyperplastic tissue granulation leading to recurrent obstruction after a median time of 112 days when FCSEMS remain in place. This rate appears to be very high in comparison with previous studies. Indeed, these studies should not be compared because almost all the stents were systematically removed in the previous studies. Bakken et al. reported 12 tissue granulations after 104 FCSEMS placements (11.5%) for benign esophageal disease (including strictures, fistulae/leaks, and perforations): seven were obstructive and five were mild. These hyperplastic reactions were described at the time of stent extraction after a mean duration of 88 days (range: 7–209), but they did not preclude stent extraction. In the series published by Eloubeidi et al., FCSEMS remained in place during 64 ± 74 days without any hyperplastic obstruction. These results underline the requirement of an early stent removal, probably 4 to 8 weeks after stent placement. In conclusion, FCSEMS provide satisfying clinical success rate with an acceptable complication rate in the management of benign esophageal strictures and they could constitute a relevant therapeutic option in this indication. Nevertheless, the use of FCSEMS does not preclude hyperplastic tissue reaction at the end of the stent, as previously reported for PCSEMS. Early removal should be systematically planned for FCSEMS to prevent complications. References 1 Spechler S J. American gastroenterological association medical statement on treatment of patients with dysphagia caused by benign disorders of the distal esophagus. Gastroenterology 1999; 117: 229–33. 2 Siersema P D. Treatment options for esophageal strictures. Nat Clin Pract Gastroenterol Hepatol 2008; 5: 142–52. 3 Pereira-Lima J C, Ramires R P, Zamin I Jr et al. Endoscopic dilation of benign esophageal strictures: report on 1043 procedures. Am J Gastroenterol 1999; 94: 1497–501. 4 Said A, Brust D J, Gaumnitz E A et al. Predictors of early recurrence of benign esophageal strictures. Am J Gastroenterol 2003; 98: 1252–6.
5 Siersema P D, Hop W C, Van Blankenstein M et al. A comparison of three types of covered metal stents for the palliation of patients with dysphagia caused by oesogastric carcinoma: a prospective, randomized study. Gastrointest Endosc 2001; 54: 145–53. 6 Conio M, Repici A, Battaglia G et al. A randomised prospective comparison of self-expandable plastic stents and partially covered self-expandable metal stents in the palliation of malignant esophageal dysphagia. Am J Gastroenterol 2007; 103: 2667–77. 7 Wadhwa R P, Kozarek R A. Use of self-expandable metallic stents in benign GI diseases. Gastrointest Endosc 2003; 58: 207–12. 8 Ackroyd R, Watson D I, Devitt P G et al. Expandable metallic stents should not be used in the treatment of benign esophageal strictures. J Gastroenterol Hepatol 2001; 16: 484–7. 9 Fiorini A, Fleischer D, Valero J et al. Self-expandable metal coil stents in the treatment of benign esophageal strictures refractory to conventional therapy: a case series. Gastrointest Endosc 2000; 52: 259–62. 10 Repici A, Conio M, De Angelis C et al. Temporary placement of an expandable polyester silicone-covered stent for treatment of refractory benign esophageal strictures. Gastrointest Endosc 2004; 60: 513–9. 11 Evrard S, Le Moine O, Lazaraki G et al. Self-expanding plastic stents for benign esophageal lesions. Gastrointest Endosc 2004; 60: 894–900. 12 Dua K S, Vleggar F P, Santharam R et al. Removable self-expanding plastic esophageal stent as a continuous, nonpermanent dilator in treating refractory benign esophageal strictures: a prospective two-center study. Am J Gastroenterol 2008; 103: 2988–94. 13 Holm A N, Baron T H. Self-expanding plastic stents in treatment of benign esophageal conditions. Gastrointest Endosc 2008; 67: 20–5. 14 Oh Y, Kochman M L, Ahmad N A, Ginsberg G G. Clinical outcomes after self-expanding plastic stent placement for refractory benign esophageal strictures. Dig Dis Sci 2010; 55: 1344–8. 15 Ogilvie A L, Dronfield M W, Ferguson R, Atkinson M. Palliative intubation of oesophagogastric neoplasms at fibreoptic endoscopy. Gut 1982; 23: 1060–7. 16 Lew R J, Kochman M L. A review of endoscopic methods of esophageal dilation. J Clin Gastroenterol 2002; 35: 117– 26. 17 Eloubeidi M A, Lopes T L. Novel removable internally fully covered self expanding metal esophageal stent: feasibility, technique of removal and tissue response in humans. Am J Gastroenterol 2009; 104: 1374–81. 18 Bakken J C, Wong Kee Song L M, de Groen P C, Baron T H. Use of a fully covered self-expandable metal stent for the treatment of benign esophageal diseases. Gastrointest Endosc 2010; 72: 712–20. 19 Sandha G S, Marcon N E. Expandable metal stents for benign esophageal obstruction. Gastrointest Endosc Clin N Am 1999; 9: 437–46. 20 Jaganmohan S, Raju G S. Tissue ingrowth in a fully covered self-expandable metallic stent (with videos). Gastrointest Endosc 2008; 68: 602–4.
© 2014 International Society for Diseases of the Esophagus
