11
ORIGINAL ARTICLE: Clinical Endoscopy Safety of endoscopic removal of self-expandable stents after treatment of benign esophageal diseases Emo E. van Halsema, MBBS, 1 Louis M. Wong Kee Song, MD, 2 Todd H. Baron, MD, FASGE, 2 Peter D. Siersema, MD, PhD, 3 Frank P. Vleggaar, MD, PhD, 3 Gregory G. Ginsberg, MD, 4 Pari M. Shah, MD, MSCE, 4 David E. Fleischer, MD, 5 Shiva K. Ratuapli, MBBS, 5 Paul Fockens, MD, PhD, FASGE, 1 Marcel G.W. Dijkgraaf, PhD, 6 Giacomo Rando, MD, 7 Alessandro Repici, MD, 7 Jeanin E. van Hooft, MD, PhD 1 Amsterdam, Utrecht, the Netherlands; Rochester, Minnesota; Philadelphia, Pennsylvania; Scottsdale, Arizona, USA; Milan, Italy Background: Temporary placement of self-expandable stents has been increasingly used for the management of benign esophageal diseases. Objective: To evaluate the safety of endoscopic removal of esophageal self-expandable stents placed for the treatment of benign esophageal diseases. Design: Multicenter retrospective study. Setting: Six tertiary care centers in the United States and Europe. Patients: A total of 214 patients with benign esophageal diseases undergoing endoscopic stent removal. Intervention: Endoscopic stent removal. Main Outcome Measurements: Endoscopic techniques for stent removal, time to stent removal, and adverse events related to stent removal. Results: A total of 214 patients underwent a total of 329 stent extractions. Stents were mainly placed for refractory strictures (49.2%) and fistulae (49.8%). Of the removed stents, 52% were fully covered self-expandable metal stents (FCSEMSs), 28.6% were partially covered self-expandable metal stents (PCSEMSs), and 19.5% were self-expandable plastic stents. A total of 35 (10.6%) procedure-related adverse events were reported, including 7 (2.1%) major adverse events. Multivariate analysis revealed that use of PCSEMSs ( P .001) was a risk factor for adverse events during stent removal. Favorable factors for successful stent removal were FCSEMSs ( P .012) and stent migration ( P .010). No significant associations were found for stent indwelling time ( P .145) and stent embedding ( P .194). Limitations: Retrospective analysis, only tertiary care centers. Conclusions: With an acceptable major adverse event rate of 2.1%, esophageal stent removal in the setting of benign disease was found to be a safe and feasible procedure. FCSEMSs were more successfully removed than self-expandable plastic stents and PCSEMSs. Adverse events caused by stent removal were not time dependent. ( Gastrointest Endosc 2013;77:18-28.) Abbreviations: CI, confidence interval; FCSEMS, fully covered self- expandable metal stent; IQR, interquartile range; OR, odds ratio; PCSEMS, partially covered self-expandable metal stent; SEMS, self- expandable metal stent; SEPS, self-expandable plastic stent. DISCLOSURE: The following author disclosed financial relationships relevant to this publication: Dr Baron: travel support from Boston Scien- tific; on the advisory board of Merit Endotek. The other authors disclosed no financial relationships relevant to this publication. See CME section; p. 108. Copyright © 2013 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2012.09.001 Received June 23, 2012. Accepted September 2, 2012. Current affiliations: Department of Gastroenterology and Hepatology (1), Academic Medical Center, Amsterdam, the Netherlands, Department of Gastroenterology and Hepatology (2), Mayo Clinic, Rochester, Minnesota, USA, Department of Gastroenterology and Hepatology (3), University Med- ical Center Utrecht, Utrecht, the Netherlands, Department of Gastroenterol- ogy and Hepatology (4), Hospital of the University of Pennsylvania, Philadel- phia, Pennsylvania, USA, Department of Gastroenterology and Hepatology (5), Mayo Clinic, Scottsdale, Arizona, USA, Clinical Research Unit (6), Aca- demic Medical Center, Amsterdam, the Netherlands, Department of Diges- tive Endoscopy (7), Istituto Clinico Humanitas, Milan, Italy. Presented at Digestive Disease Week, May 19-22, 2012, San Diego, California (Gastrointest Endosc 2012;75:AB168-9; Gastrointest Endosc 2012;75:AB458). Reprint requests: Jeanin E. van Hooft, MD, PhD, Department of Gastroenter- ology and Hepatology, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, the Netherlands. If you would like to chat with an author of this article, you may contact Dr van Hooft at [email protected]. 18 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013 www.giejournal.org

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ORIGINAL ARTICLE: Clinical Endoscopy

Safety of endoscopic removal of self-expandable stents after treatmentof benign esophageal diseases

Emo E. van Halsema, MBBS,1 Louis M. Wong Kee Song, MD,2 Todd H. Baron, MD, FASGE,2

Peter D. Siersema, MD, PhD,3 Frank P. Vleggaar, MD, PhD,3 Gregory G. Ginsberg, MD,4

Pari M. Shah, MD, MSCE,4 David E. Fleischer, MD,5 Shiva K. Ratuapli, MBBS,5

Paul Fockens, MD, PhD, FASGE,1 Marcel G.W. Dijkgraaf, PhD,6 Giacomo Rando, MD,7

Alessandro Repici, MD,7 Jeanin E. van Hooft, MD, PhD1

Amsterdam, Utrecht, the Netherlands; Rochester, Minnesota; Philadelphia, Pennsylvania; Scottsdale, Arizona, USA; Milan, Italy

Background: Temporary placement of self-expandable stents has been increasingly used for the managementof benign esophageal diseases.

Objective: To evaluate the safety of endoscopic removal of esophageal self-expandable stents placed for thetreatment of benign esophageal diseases.

Design: Multicenter retrospective study.

Setting: Six tertiary care centers in the United States and Europe.

Patients: A total of 214 patients with benign esophageal diseases undergoing endoscopic stent removal.

Intervention: Endoscopic stent removal.

Main Outcome Measurements: Endoscopic techniques for stent removal, time to stent removal, and adverseevents related to stent removal.

Results: A total of 214 patients underwent a total of 329 stent extractions. Stents were mainly placed for refractory strictures(49.2%) and fistulae (49.8%). Of the removed stents, 52% were fully covered self-expandable metal stents (FCSEMSs), 28.6%were partially covered self-expandable metal stents (PCSEMSs), and 19.5% were self-expandable plastic stents. A total of 35(10.6%) procedure-related adverse events were reported, including 7 (2.1%) major adverse events. Multivariate analysisrevealed that use of PCSEMSs (P � .001) was a risk factor for adverse events during stent removal. Favorable factors forsuccessful stent removal were FCSEMSs (P � .012) and stent migration (P � .010). No significant associations were foundfor stent indwelling time (P � .145) and stent embedding (P � .194).

Limitations: Retrospective analysis, only tertiary care centers.

Conclusions: With an acceptable major adverse event rate of 2.1%, esophageal stent removal in the setting ofbenign disease was found to be a safe and feasible procedure. FCSEMSs were more successfully removed thanself-expandable plastic stents and PCSEMSs. Adverse events caused by stent removal were not time dependent.(Gastrointest Endosc 2013;77:18-28.)

Abbreviations: CI, confidence interval; FCSEMS, fully covered self-expandable metal stent; IQR, interquartile range; OR, odds ratio;PCSEMS, partially covered self-expandable metal stent; SEMS, self-expandable metal stent; SEPS, self-expandable plastic stent.

DISCLOSURE: The following author disclosed financial relationshipsrelevant to this publication: Dr Baron: travel support from Boston Scien-tific; on the advisory board of Merit Endotek. The other authors disclosedno financial relationships relevant to this publication.

See CME section; p. 108.

Copyright © 2013 by the American Society for Gastrointestinal Endoscopy0016-5107/$36.00http://dx.doi.org/10.1016/j.gie.2012.09.001

Received June 23, 2012. Accepted September 2, 2012.

Current affiliations: Department of Gastroenterology and Hepatology (1),

Gastroenterology and Hepatology (2), Mayo Clinic, Rochester, Minnesota,USA, Department of Gastroenterology and Hepatology (3), University Med-ical Center Utrecht, Utrecht, the Netherlands, Department of Gastroenterol-ogy and Hepatology (4), Hospital of the University of Pennsylvania, Philadel-phia, Pennsylvania, USA, Department of Gastroenterology and Hepatology(5), Mayo Clinic, Scottsdale, Arizona, USA, Clinical Research Unit (6), Aca-demic Medical Center, Amsterdam, the Netherlands, Department of Diges-tive Endoscopy (7), Istituto Clinico Humanitas, Milan, Italy.

Presented at Digestive Disease Week, May 19-22, 2012, San Diego,California (Gastrointest Endosc 2012;75:AB168-9; Gastrointest Endosc2012;75:AB458).

Reprint requests: Jeanin E. van Hooft, MD, PhD, Department of Gastroenter-ology and Hepatology, Academic Medical Center, Meibergdreef 9, 1105 AZAmsterdam, the Netherlands.

If you would like to chat with an author of this article, you may contact Dr van

Academic Medical Center, Amsterdam, the Netherlands, Department of Hooft at [email protected].

18 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013 www.giejournal.org

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Until recently, esophageal stents were mainly used forthe palliative treatment of malignant dysphagia.1 To en-ure stent patency for the remaining lifetime of the patient,tent design has focused on prevention of migration andecurrent obstruction. The indications for stent placementradually widened to include treatment of benign esoph-geal diseases, such as fistulae and complex strictures.2,3

Stents for benign diseases are not intended to be perma-nent, and safe removal is an essential feature. Uncoveredand partially covered stents are difficult to remove becauseof stent embedding and granulation tissue, which occurafter prolonged stent periods.4-6 Conversely, fully coveredstents migrate more often because the covering preventsembedding in the tissue.2 Although there are reports ofuccessful retrieval of migrated stents,7,8 one can imaginehat stent migration might make stent removal difficult.

In addition to tissue responses and stent migration,ther serious stent-related adverse events include fistulaormation and stent erosion into the esophageal wall, withesultant perforation and major bleeding.6,9-13 These latter

adverse events can also occur during stent removal.4,14-19

To prevent adverse events in patients with benign esoph-ageal disease, stent removal is recommended within 6weeks after insertion. However, this recommendation isbased on data from a small case series.4

Although there is consensus on the necessity to removeesophageal stents in patients with benign esophageal dis-ease, little is known about the safety of removal and theideal stent indwelling time to prevent adverse events. Thisretrospective multicenter study was designed to examinethe safety of esophageal stent removal in patients withbenign esophageal disease and to assess the effect of stentindwelling time on adverse events during removal.

PATIENTS AND METHODS

This retrospective multicenter study was conducted at 6tertiary care centers in the United States and Europe. Theresearch protocol was approved by the institutional re-view board of each participating center. Patients whounderwent esophageal stent placement between May 2002and August 2011 were identified by search of the elec-tronic medical database at each center. Patients were in-cluded in the study if they received a temporary esopha-geal stent proximal to or bridging the gastroesophagealjunction or surgical anastomosis for benign disease. Exclu-sion criteria included patients with active malignantesophageal disease or if the stent was not removed for thefollowing reasons: patient was lost to follow-up, was unfitfor stent removal, died with the stent in situ, or received abiodegradable stent as primary treatment for a benignesophageal lesion. Adverse events related to stent extrac-tion were recorded during a follow-up period of 30 daysafter the procedure. Informed consent was obtained from

all patients. w

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ata collectionData were abstracted for patient demographics, indica-

ion for stent placement, dates of stent insertion and re-oval, stent location, characteristics of the stent placed

type, length, and body diameter), technique for stentemoval, and adverse events. The location of the stent wasategorized as positioned in the proximal segment (�25m from the incisors), middle segment (25-30 cm from thencisors), or distal segment (�30 cm from the incisors) ofhe esophagus. To compare outcomes as a function oftent length, patients were classified into 3 groups basedn the overall median stent length: (1) shorter than 10 cm,2) 10 to 12 cm, and (3) longer than 12 cm. Similarly, aomparison among 3 groups of patients was performedased on stent body diameter: (1) less than 20 mm, (2) 20o 22 mm, and (3) more than 22 mm. The stent indwellingimes were divided into quartiles. Successful stent removalas defined as endoscopic stent retrieval at the first at-

empt without the occurrence of stent-related adversevents during or within 30 days of the procedure. Thetent-in-stent procedure was considered to be primarytent removal because stent extraction was attempted afterlacement of a second stent inside the embedded stent.econdary removal was defined as endoscopic failure oftent removal during the first attempt. Adverse events wereefined as any adverse event related to stent extractionhat occurred within 30 days of the procedure. Adversevents were graded as major if surgical intervention wasequired, the continuity of the esophagus was interrupted,leeding occurred that required intervention, and othervents resulting in serious consequences for the patientdeath, life threatening, persistent significant disability).dverse events without the need for intervention wereraded as minor.

tatistical analysisData analysis was performed on a per-procedure rather

han per-patient basis because previous esophageal stentemoval procedures in our patient population were notssociated with an increased risk of removal-related ad-erse events (P � .644). To analyze stent indications asotential risk factors for complicated stent removal, they

Take-home Message

● Endoscopic removal of self-expandable stents is feasibleand relatively safe, with a major adverse event rate of2.1%. Fully covered self-expandable metal stents (SEMSs)were associated with a lower rate of stent removal–related adverse events than partially covered SEMSs orself-expandable plastic stents.

● The stent indwelling time was not a significant factor withregard to adverse events related to stent removal.

ere divided into 4 major groups because of great heter-

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Esophageal stent removal van Halsema et al

TABLE 1. Baseline characteristics of 329 stent removals

Characteristic Total (%)

Stent removals by center

Academic Medical Center 25 (7.6)

Hospital of the University ofPennsylvania

35 (10.6)

Istituto Clinico Humanitas 52 (15.8)

Mayo Clinic Rochester 161 (48.9)

Mayo Clinic Scottsdale 17 (5.2)

University Medical Center Utrecht 39 (11.9)

Sex, N � 214

Male 143 (66.8)

Female 71 (33.2)

Age, y, mean � SD (range) 58 � 14.6 (11–94)

Multiple stent removals

No 142 patients (66.4)

Yes 72 patients (33.6)

Median stent removals per patient(range)

1 (1–7)

Overlapping stents

No 300 (91.2)

Yes 29 (8.8)

Indications for stent placement

Benign strictures 162 (49.2)

Benign fistulae/leaks/perforations 164 (49.8)

Missing data/unknown 3 (0.9)

Stent location

Proximal esophagus (�25 cm) 147 (44.7)

Mid-esophagus (25-30 cm) 72 (21.9)

Distal esophagus (�30 cm) 109 (33.1)

Missing data/unknown 1 (0.3)

Stent indwelling time, d

Median (range) 37 (0–659)

�21 84 (25.5)

21-37 79 (24.0)

38-77 84 (25.5)

�77 80 (24.3)

Missing data/unknown 2 (0.6)

SD, Standard deviation.

20 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013

TABLE 2. Stent characteristics (N � 329)

Characteristic Total (%)

Fully covered SEMS

Alimaxx-E (Alveolus) 79 (24.0)

Bonastent (Endochoice) 1 (0.3)

Choostent (M.I. Tech) 2 (0.6)

Esophageal Z (Cook Medical) 1 (0.3)

Evolution (Cook Medical) 3 (0.9)

FerX-Ella (Ella-CS) 1 (0.3)

Flamingo Wallstent (Boston Scientific) 1 (0.3)

Hanarostent colonic (M.I. Tech) 5 (1.5)

Niti-S (Taewoong Medical) 7 (2.1)

Tracheal SEMS 2 (0.6)

Viabil biliary stent (Gore) 4 (1.2)

Wallflex (Boston Scientific) 65 (19.8)

Partially covered SEMSs

Ultraflex (Boston Scientific) 78 (23.7)

Wallflex (Boston Scientific) 4 (1.2)

Gianturco Z (Cook Medical) 1 (0.3)

Evolution (Cook Medical) 9 (2.7)

Tracheal SEMSs 2 (0.6)

SEPSs

Polyflex (Boston Scientific) 64 (19.5)

Stent covering

Fully covered SEMSs 171 (52.0)

Partially covered SEMSs 94 (28.6)

SEPSs 64 (19.5)

Stent length, cm

Median (range) 10.0 (4.0–15.5)

�10.0 81 (24.6)

10.0–12.0 213 (64.7)

�12.0 26 (7.9)

Missing 9 (2.7)

Stent diameter, mm

Median (range) 20 (10–28)

�20 146 (44.4)

20–22 73 (22.2)

�22 87 (26.4)

Missing 23 (7.0)

SEMSs, Self-expandable metal stents; SEPSs, self-expandable plastic stents.

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van Halsema et al Esophageal stent removal

ogeneity. The Mann-Whitney U test was used to comparestent indwelling times between uncomplicated and com-plicated stent removal. Binary logistic regression was usedto identify other risk factors for complicated stent removal.Potential risk factors with P � .1 from univariate analysiswere included in a backward multivariate logistic regres-sion model. Multivariate analysis of 304 procedures wasperformed, excluding the 25 cases in which informationon stent diameter or indication for stent placement wasmissing. Statistics are presented as P value with corre-sponding odds ratio (OR) and 95% confidence interval(CI). P values �.05 were considered statistically signifi-cant. Continuous variables are presented as mean � stan-dard deviation, median with the interquartile range (IQR),or the lowest and highest value (range). Statistical analyseswere performed with the SPSS software package PASWStatistics 18.0 (IBM Corp, Armonk, NY).

RESULTS

The study cohort consisted of 214 patients (143 [66.8%]males) who underwent a total of 329 esophageal stentplacements for benign disease with subsequent stent re-moval. The baseline characteristics of the study populationare summarized in Table 1. At the time of stent insertion,

TABLE 3. Removal-related adverse events

Adverse eventsOverall (N � 329),

no. (%)

Minor

Minor bleeding 16 (4.9)

Severe pain 6 (1.8)

Fracture of stent 2 (0.6)

Ulceration 1 (0.3)

Mucosal tear 2 (0.6)

Unsuccessful first attempt 1 (0.3)

Total 28 (8.5)

Major

Perforation 3 (0.9)

Esophageal avulsion 1 (0.3)

Stridor requiring endotracheal intubation 1 (0.3)*

Surgical removal 1 (0.3)

Fistula formation 1 (0.3)

Total major adverse events 7 (2.1)

Total 35 (10.6)

*Fractured stent.

the mean patient age was 58 � 14.6 years (range 11-94 2

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ears). Indications for esophageal stent placement in-luded benign strictures (n � 162; 49.2%), benign fistulae/eaks/perforations (n � 164; 49.8%), and unknown (n � 3;.9%). The median number of stent removals per patientas 1 (range 1-7 removals).Characteristics of the stents used in the study are sum-

arized in Table 2. The majority of stents placed wereelf-expandable metal stents (SEMSs) (n � 265; 80.5%).he SEMSs were either fully covered (n � 171) or partiallyovered (n � 94). The median stent length was 10 cmrange 4.0-15.5 cm), and the median diameter was 20 mmrange 10-28 mm). Stent-related adverse events were re-orted in 122 patients (37.1%), including migration (n �1; 27.7%), severe embedding by granulation tissue (n �4; 4.3%), stent-induced fistulae (n � 8; 2.4%), stent-nduced stenosis (n � 5; 1.5%), severe pain requiringemoval (n � 2; 0.6%), stridor requiring removal (n � 1;.3%), and pressure necrosis (n � 1; 0.3%).

tent indwelling times and removalechniques

A total of 329 stents were removed after an overalledian indwelling time of 37 days (IQR 20-77 days). With

egard to stent type, the median indwelling time was 45ays (IQR 23-84 days) for fully covered SEMSs (FCSEMSs),

tent migration� 91), no. (%)

Stent embedding(n � 14), no. (%)

Remaining group(n � 224), no. (%)

— 3 (21.4) 13 (5.8)

— — 6 (2.7)

— — 2 (0.9)

— — 1 (0.4)

— — 2 (0.9)

— — 1 (0.4)

— 3 (21.4) 25 (11.2)

— — 3 (1.3)

— — 1 (0.4)

— — 1 (0.4)

1 (1.1) — —

— — 1 (0.4)

1 (1.1) 6 (2.7)

1 (1.1) 3 (21.4) 31 (13.8)

S(n

5 days (IQR 15-44 days) for partially covered SEMSs

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Esophageal stent removal van Halsema et al

TABLE 4. Univariate analysis of removal-related adverse events

No adverse events(n � 294)

Adverse events(n � 35) OR (95% CI) P value

Hosts

Male 210 (91.3) 20 (8.7) Reference

Female 84 (84.8) 15 (15.2) 1.875 (0.917–3.835) .085

Age, y, mean � SD (range) 58 � 15 (11–94) 56 � 12 (36–87) 0.990 (0.967–1.013) .378

Stenting indications .096

Radiation-induced strictures 37 (82.2) 8 (17.8) Reference

Anastomotic strictures 71 (94.7) 4 (5.3) 0.261 (0.074–0.923) .037

Miscellaneous strictures 40 (95.2) 2 (4.8) 0.231 (0.046–1.160) .075

Fistulae/leakages/perforations 143 (87.2) 21 (12.8) 0.679 (0.279–1.656) .395

Missing 3 0

Stent location in esophagus .774

Proximal segment 131 (89.1) 16 (10.9) Reference

Middle segment 63 (87.5) 9 (12.5) 1.170 (0.490–2.792) .724

Distal segment 99 (90.8) 10 (9.2) 0.827 (0.360–1.901) .655

Missing 1 0

Stent material

Metal 236 (89.1) 29 (10.9) 1.188 (0.471–2.995) .715

Plastic 58 (90.6) 6 (9.4) Reference

Stent covering .000

Fully covered 165 (96.5) 6 (3.5) Reference

Partially covered 71 (75.5) 23 (24.5) 8.908 (3.478–22.818) .000

SEPS 58 (90.6) 6 (9.4) 2.845 (0.883–9.170) .080

Stent length, cm .775

�10.0 73 (90.1) 8 (9.9) Reference

10-12 188 (88.3) 25 (11.7) 1.213 (0.523–2.813) .652

� 12.0 24 (92.3) 2 (7.7) 0.760 (0.151–3.830) .740

Missing 9 0

Stent diameter, mm .002

�20 135 (92.5) 11 (7.5) Reference

20-22 70 (95.9) 3 (4.1) 0.526 (0.142–1.947) .336

�22 69 (79.3) 18 (20.7) 3.202 (1.433–7.155) .005

Missing 20 3

Overlapping stents

No 268 (89.3) 32 (10.7) Reference

Yes 26 (89.7) 3 (10.3) 0.966 (0.277–3.373) .957

(Table continued on next page)

22 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013 www.giejournal.org

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van Halsema et al Esophageal stent removal

(PCSEMSs), and 49 days (IQR 15-94 days) for self-expandable plastic stents (SEPSs). PCSEMSs were removedearlier than FCSEMSs (P � .001) and SEPSs (P � .003).Primary removal was achieved in 326 procedures (99.1%),including 12 stent-in-stent procedures (3.6%), and second-ary removal was achieved in the remaining 3 (0.9%). Stentswere removed endoscopically by traction pull using asingle grasping forceps (n � 284; 86.3%), by the stent-in-stent technique (n � 12; 3.6%), by a snare-assistedechnique (n � 7; 2.1%), with other endoscopic instru-ents (n � 3; 0.9%), or by argon plasma coagulation (n �

2; 0.6%); the removal technique was unknown in 18(5.5%) removals. A rendezvous procedure through a mini-gastrotomy was performed in 2 cases (0.6%) to allow distalaccess because of a tight stricture proximal to the stent.One stent was removed surgically after failed endoscopicextraction. Embedded stents were removed after a medianof 47 days (range 25-539 days) compared with 35 days(range 0-659 days) when no significant embedding wasreported (P � .031). When the stent-in-stent techniquewas used, a second stent was placed within the lumen ofthe embedded stent to induce pressure necrosis of gran-ulation tissue ingrowth or overgrowth. Seven biodegrad-able stents, 4 FCSEMSs, and 1 SEPS were used as secondstents. Both stents were removed as one using a graspingforceps after a median indwelling time of 10 days (range

TABLE 4. (Continued)

No adverse event(n � 294)

Multiple stent removals

No 190 (88.8)

Yes 104 (90.4)

Stent indwelling time, d

�21 74 (88.1)

21-36 67 (84.8)

37-77 76 (90.5)

�77 75 (93.8)

Missing 2

Stent migration

No 204 (85.7)

Yes 90 (98.9)

Stent embedding by granulation tissue

No 283 (89.8)

Yes 11 (78.6)

OR, Odds ratio; CI, confidence interval; SD, standard deviation; SEPS, self-expan

6-21 days), excluding 1 exceptional case with an indwell- t

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ng time of 431 days in an 87-year-old patient with a peptictricture.

dverse events related to stent removalA total of 35 stent removal–related adverse events

10.6%) were reported, including 28 minor (8.5%) and 7ajor (2.1%) adverse events, which are summarized inable 3. Removal-related adverse events occurred after aedian stent indwelling time of 29 days (range 2-193 days)

ompared with 39 days (range 0-659 days) for the uncom-licated group (P � .145). The median stent indwellingimes for minor and major adverse events were not signif-cantly different (P � .360) and were 23.5 days (range-138 days) and 32 days (range 22-193 days), respectively.hen adjusting for stent type, complicated removal was

ot associated with prolonged stent indwelling times. Theedian stent indwelling times for complicated versus un-

omplicated removal of FCSEMSs were 45 days (range-138 days) versus 45 days (range 1-391 days), respectivelyP � .672), 30 days (range 9-193 days) versus 23 daysrange 0-539 days), respectively (P � .066) for PCSEMSemoval, and 10.5 days (range 2-52 days) versus 51.5 days1-659 days), respectively (P � .036) for SEPS removal.omplicated SEPS removal, including severe pain (n � 4),econdary removal (n � 1), and fistula (n � 1), occurredfter a significantly shorter median stent indwelling time

Adverse events(n � 35) OR (95% CI) P value

24 (11.2) Reference

11 (9.6) 0.837 (0.394–1.777) .644

.329

10 (11.9) Reference

12 (15.2) 1.325 (0.538–3.266) .540

8 (9.5) 0.779 (0.291–2.082) .619

5 (6.3) 0.493 (0.161–1.513) .216

0

34 (14.3) Reference

1 (1.1) 0.067 (0.009–0.495) .008

32 (10.2) Reference

3 (21.4) 2.412 (0.639–9.101) .194

plastic stent.

s

han the uncomplicated group. This finding, which con-

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Esophageal stent removal van Halsema et al

tradicts the hypothesis, does not imply any consequencesfor clinical practice and was therefore not relevant. Nostent-related mortality was observed in this retrospectiveseries of patients.

On univariate analysis (Table 4), a significant associa-tion was found between the occurrence of stent removal–related adverse events and the use of PCSEMSs and large-diameter (�22 mm) stents. The removal of PCSEMSs wassignificantly more traumatic than removal of FCSEMSs (Ta-ble 4) and SEPSs (OR 3.13; 95% CI, 1.20-8.20). Stentsplaced for an anastomotic stricture were more successfullyremoved than stents placed for a radiation-induced stric-ture. Stent migration was a favorable factor for safer stentremoval. No significant associations were found for thefollowing variables: patient’s sex and age, stent location,stent material, stent length, overlapping stents, multiplestent removals, stent indwelling time, and stent embed-ding by granulation tissue.

Multivariate analysis was performed with the followingvariables: stent covering, stent indication, stent migration,stent diameter, and patient’s sex. PCSEMSs were associ-ated with complicated removal compared with FCSEMSs(OR 8.83; 95% CI, 3.29-23.70) and SEPSs compared withFCSEMSs (OR 4.71; 95% CI, 1.39-15.97). Stent migrationwas associated with a successful outcome (OR 0.07; 95%CI, 0.01-0.54). No significant association was found forfemale sex (OR 2.17; 95% CI, 0.93-5.05), large-diameterstents (OR 1.92; 95% CI, 0.71-5.16), and anastomotic stric-tures (OR 0.43; 95% CI, 0.11-1.72). Stents placed forfistulae/perforations tended to be removed more easilythan stents placed for radiation-induced strictures (OR0.32; 95% CI, 0.09-1.09).

DISCUSSION

To our knowledge, this retrospective study is the largestseries on the technical success and adverse events relatedto stent removal in the setting of benign esophageal dis-ease. In our series, endoscopic removal of self-expandablestents from the esophagus after treatment of benign dis-ease was a feasible and safe procedure, with a majoradverse event rate of 2.1% and an overall adverse eventrate of 10.6% (Figs. 1-3).) These results are similar topublished rates of adverse events related to stent removalfrom 3 smaller series.4,5,14 Two of these series, however,also included malignant indications.5,14 Van Heel et al5

reported on stent removal complicated by adverse eventsin 11.3% (14/124) of cases after extraction of both PC-SEMSs (68%) and FCSEMSs (32%). Yoon et al14 described

procedure-related adverse event rate of 5.9% (7/119),ncluding fatal major bleeding in 1 patient. The latter seriesncluded FCSEMSs only, which might explain the relativelyower adverse event rate. A third case series comparedemoval of both PCSEMSs and FCSEMSs after short-termtenting (�6 weeks) with removal after long-term stenting

�6 weeks) as a secondary endpoint.4 Adverse events p

24 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013

ccurred in 15.2% (5/33) of cases, all in the long-termtenting group. More recent studies reported on successfultent extraction in the majority of cases in the setting ofenign esophageal disease, although stent removal wasot a focus of these studies.6-8,17,18,20-22

In our series, 7 patients experienced major adversevents related to stent removal, the details of which are

igure 1. A, A fully covered Choostent (M.I. Tech) placed for a strictureecondary to radiofrequency ablation after 54 days of stent therapy. B,he stent was removed by inversion by traction pull with graspingorceps at the distal loop. C, Granulation tissue growth was present at theistal end of the stent.

resented in Table 5. Esophageal disruption and perfora-

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van Halsema et al Esophageal stent removal

tion were the most significant risks associated with stentextraction and were only seen with PCSEMSs. Traumaticremoval of PCSEMSs has also been reported by othergroups.5,16 Other adverse events, such as intramural rup-ture, fistula formation, and segmental amputation of theesophagus, have also been described with the extractionof FCSEMSs.14,18,19 We experienced 1 major adverse eventafter removal of a SEPS; a fistula was visualized on upperendoscopy on the same day and was thought to be anadverse event of stent placement rather than related to thestent removal procedure. Traumatic SEPS removal mayoccur less frequently because of the lower incidence ofstent embedding.23 However, severe stent embedding hasbeen reported with the use of these devices.7,8,10,24 Wencountered 3 cases (0.9%) of stent fracture (2 FCSEMSsnd 1 PCSEMS) during the removal procedure, whichesulted in 1 major adverse event. Van Heel et al5 reported

stent fracture in 5 cases (4%) that led to life-threateningadverse events in 2 patients from the nonremovable stent

Figure 2. A, Two overlapping partially covered Ultraflex stents (BostonScientific), placed for a perforation and anastomotic stricture, after, re-spectively, 69 and 45 days of stent therapy. B, Removal by traction pullwith grasping forceps during the same procedure was uncomplicated.

fragments. l

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Similar to other series, removal of PCSEMSs was asso-iated with significantly more adverse events thanCSEMSs or SEPSs. Still, some prefer to use PCSEMSsecause they seem to be less likely to migrate.3,17 Theame process that minimizes stent migration (ie, tissuembedding in the uncovered portions of the stent) alsoenders removal more difficult and traumatic.3 In our se-ies, 14 stents (4.3%), including 12 PCSEMSs and 2 FC-EMSs, were removed after they were found to be severelymbedded by granulation tissue. The majority of thesembedded stents were removed successfully by the stent-n-stent technique with a median indwelling time of 10ays for the second stent. Successful removal by using thetent-in-stent technique was the focus of 2 other series inhich the second stent was left in situ for a median time of2 and 14 days.6,15 Aside from the occurrence of 3 self-

igure 3. A, A partially covered Ultraflex stent (Boston Scientific) after 41ays of stent therapy with the presence of moderate granulation tissuerowth through the uncovered parts of the stent. B, Removal by tractionull with grasping forceps resulted in self-limiting bleeding.

imiting bleeding events, embedded stents were not sig-

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Esophageal stent removal van Halsema et al

nificantly associated with major adverse events duringstent removal in our series. Swinnen et al6 support thesefindings as successful stent removal was achieved in 97.8%(132/135) of cases, including 73.3% stent-in-stent proce-dures because of the presence of moderate to severe tissuehyperplasia. Other smaller series have shown that stentscomplicated by tissue ingrowth or overgrowth can beremoved successfully,22,24 although in a small proportionof cases, embedded stents may need to be left in situ orrequire surgical removal.5,8,17

In addition to stent covering, it is speculated that gran-ulation tissue growth can be related to stent size and radialforce.3 In our series, we did not find an association be-tween stent size and removal outcome, nor when compar-ing the median stent sizes of the complicated group withthe uncomplicated group. These findings are similar tothose of the series by van Heel et al.5

In our series, 91 stents (27.7%) were removed after theyhad migrated, the majority of which (85.7%) were re-trieved from the stomach (Fig. 4). Except for the occurrenceof 1 major adverse event, stent migration was found to be afavorable factor for successful stent removal. Safe stent re-trieval after migration has also been reported by othergroups,7,8,14 although some distally migrated stents (eg, in themall bowel) may require surgical removal.10,18,25-28

A prolonged stent indwelling time is thought to com-

TABLE 5. Major adverse events during stent removal

PtSex/age,

y IndicationLocation

esophagus Stent type co

1 F/48 Fistula after Roux-en-Y gastricbypass

Distal Evolution 150 �20 mm

P

2 M/59 Fistula �anastomoticstricture

Proximal Ultraflex 120 �23 mm

P

3 M/43 Anastomoticstricture

Proximal Ultraflex 120 �23 mm

P

4 F/70 Anastomoticleakage

Distal Ultraflex 120 �(md) mm

P

5 F/52 Perforation Distal Ultraflex 120 �23 mm

P

6 M/61 Boerhaavesyndrome

Distal Ultraflex 120 �28 mm

P

7 M/63 Radiation-inducedstricture

Proximal Polyflex* 120 �16 mm

F

Pt, Patient; F, female; M, male; md, missing data; APC, argon plasma coagulatio*Self-expandable plastic stent.

plicate stent removal because of granulation tissue in- s

26 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013

rowth and overgrowth. However, there are few data toupport this assumption. Some studies suggest an associ-tion between prolonged stent indwelling time and theccurrence of stent embedding by granulation tissue.6,29 Inur series, severe embedding was seen after a median of5 days (range 14-323 days), and embedded stents re-ained in situ significantly longer, so the occurrence of

tent embedding may be time dependent. However, stentmbedding can already be seen after 14 days and is eveneported to occur within 7 days.30,31 The issue remainshether stent embedding is associated with complicated

emoval. Two studies demonstrated that the outcome oftent removal is time dependent and stent removal isecommended within 6 weeks.4,5 In both series, removal-elated adverse events occurred because of stent embed-ing, which can be explained by the high proportion ofCSEMSs that were used in these studies. As mentionedreviously, the evidence suggests that the safest approachs to use the stent-in-stent technique to remove embeddedtents. However, in both studies, the stent-in-stent tech-ique was rarely used. In our series, complicated removalas not found to be time dependent, and 75 stents (22.8%)ere successfully removed, even after a minimum stent

ndwelling time of 79 days (median 113 days, range 79-659ays). An explanation for this finding could be that when

gDwell

time, d Removal technique Adverse events

35 Esophagojejunostomy Stent had migrated distally. Distalflare was found embedded injejunum, requiring surgicalremoval

193 Grasping forceps Esophageal avulsion

32 Grasping forceps byinvagination of stent,APC, and overtubeassistance

Stent difficult to negotiate,multiple passages of endoscope,stent fracture. Stridor developedin patient caused by edema fromtrauma requiring endotrachealintubation

22 Grasping forceps byinvagination of stent

Perforation

32 Missing data Perforation

29 Grasping forceps byinvagination of stent

Perforation

49 Grasping forceps Fistula-to-anterior cervical plate;discovered after stent removal,probably stent induced

Stentverin

artially

artially

artially

artially

artially

artially

ully

n.

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van Halsema et al Esophageal stent removal

in-stent technique for stent removal. Successful stent re-moval after long-term stenting has been described.32,33

This study has some limitations. First, follow-up wasrelatively short after stent removal. Second, the retrospec-tive multicenter design includes inherent limitations, suchas heterogeneous data because of differences in patientpopulations, endoscopic techniques, stent designs, andclinical assessment. Adverse events were not predefinedand were recorded based on the endoscopist’s report ofthe removal procedure or during follow-up. There is se-

Figure 4. A, A partially covered Ultraflex stent (Boston Scientific) mi-grated into the stomach and was removed after 32 days (B) withoutadverse events (C).

lection bias because only cases in which stent removal was

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ttempted were included. In cases in which the endosco-ist decided, for whatever reason, not to remove a stenthat was initially placed as temporary treatment, then theatient did not meet inclusion criteria. Third, the high ratiof the number of variables to the number of study out-omes may have resulted in an overfitting multivariateogistic regression model. To assess the impact of possibleverfitting, we performed a penalized multivariate logisticegression analysis by the LASSO (least absolute shrinkagend selection operator) method. Stent covering turned outo be the strongest predictor; removal of PCSEMSs wasore complicated than removal of FCSEMSs (OR 8.83;

5% CI, 3.38-23.06), and the same applied for the removalf SEPSs (OR 3.18; 95% CI, 0.98-10.30). All other variablesere dropped. Fourth, data were analyzed per procedure

ather than per patient. To account for any bias resultingrom multiple stent removals in patients, we performed annalysis following a generalized estimating equation ap-roach. Again, stent covering was the strongest predictor;ompared with removal of FCSEMSs, PCSEMS removalas more complicated (OR 6.74; 95% CI, 2.03-22.41) asas SEPS removal (OR 4.32; 95% CI, 1.15-16.25). Again, nother variables were selected. Identifying stent covering ashe strongest predictor, the results of these additionalASSO and generalized estimating equation analyses areonsistent with the results of the reported logistic regres-ion. Stent migration, however, was no longer identified aspredictor in either of the additional analyses, possibly

ecause partially covered stents migrate less easily. Con-idering this undetermined outcome, we suggest that theredictive role of stent migration needs further research.In conclusion, this large series demonstrates that re-

oval of self-expandable stents after treatment of be-ign esophageal disease is a safe and feasible proce-ure. Adverse events caused by stent removal occurredess frequently when FCSEMSs, rather than SEPSs andCSEMSs, were used. The stent-in-stent techniqueeems to be a safe approach for removal of significantlymbedded stents.

CKNOWLEDGMENTS

We thank Daisy Walter, MD, from the University Med-cal Center Utrecht, and Michael L. Kochman, MD, fromhe Hospital of the University of Pennsylvania, for theirontribution and dedicated work on data collection. Spe-ial thanks to Dr ir. Michael W.T. Tanck, genetic epidemi-logist and biostatistician at the Academic Medical Center,niversity of Amsterdam, for all his efforts and very valu-ble assistance with the statistics.

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