9

Click here to load reader

Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

Embed Size (px)

Citation preview

Page 1: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

R

Eo

Na

b

a

ARAA

KACEE

1

airbfa

soCm(eltc

pi

T

1h

Digestive and Liver Disease 46 (2014) 195–203

Contents lists available at ScienceDirect

Digestive and Liver Disease

jou rna l h om epage: www.elsev ier .com/ locate /d ld

eview Article

ndoscopic treatment of iatrogenic gastrointestinal perforations: Anverview

ajib Al Ghossainia, Damien Lucidarmea, Philippe Buloisb,∗

Department of Digestive Diseases, University Nord de France, Lille, FranceHôpital Privé La Louvière, Générale de Santé, Lille, France

r t i c l e i n f o

rticle history:eceived 1 March 2013ccepted 10 September 2013vailable online 8 November 2013

eywords:

a b s t r a c t

In the past, the treatment of iatrogenic gastrointestinal perforations was limited to surgical managementor to medical observation. Natural Orifice Transluminal Endoscopic Surgery (NOTES) has paved the waytowards the development of reliable endoscopic closure techniques, which can be applicable in accidentalperforations of the gastrointestinal tract.

When endoscopic treatment is feasible, hemoclips are preferred in smaller perforations, while over-

cute perforationlipndoscopic complicationndoscopic repair

the-scope-clips or a combination of hemoclips, endoloops, and glue are used in larger ones. Endoscopicstitching is rarely utilized, and endoscopic stapling has been practically abandoned. The use of self-expandable covered stents can be considered in the esophagus and duodenum. Broad spectrum antibioticsare recommended in most cases. Clinical follow-up in a medico-surgical unit is mandatory and surgicalintervention should not be delayed more than 24 h if clinical or biological worsening occurs. Imaging withoral contrast medium is advisable before resumption of oral feeding in the case of large perforations.

Gast

© 2013 Editrice

. Introduction

Recent advances in interventional endoscopy have provided anlternative to surgery by affording a minimally invasive approachn selected patients. However, some of these procedures carry aisk of iatrogenic perforation (IP). Traditionally, treatment of IP haseen limited to surgical management or to medical observation;ortunately, many of these complications can now be treated safelynd effectively with endoscopy.

Iatrogenic perforation can often be recognized during the endo-copic procedure itself, either by direct visualization of the adjacentrgans, or by sudden loss of lumen distension despite insufflation.losing the perforations, which appear secondary to endoscopicucosal resection (EMR) or endoscopic submucosal dissection

ESD), is often simpler than those which occur during diagnosticndoscopy, as the latter result from blunt trauma and are often tooarge to be treated endoscopically [1]. It is advisable to carry onhe endoscopic repair immediately in order to prevent peritonealontamination.

Endoscopic techniques, such as clipping, stenting, suturing, sta-ling, and combining clips with loops and glue, have been described

n the literature.

∗ Corresponding author at: 20 rue du Ballon, F-59000 Lille, France.el.: +33 32056969; fax: +33 320576947.

E-mail address: [email protected] (P. Bulois).

590-8658/$36.00 © 2013 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevierttp://dx.doi.org/10.1016/j.dld.2013.09.024

roenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.

The aim of this article is to review the available data on endo-scopic closure of IP, focusing on their incidence, mechanisms, andrisk factors, trying to suggest step-up algorithms of endoscopictreatment, followed, in the case of failure, by timely surgical man-agement. Nevertheless, most endoscopic treatments are the resultof anecdotal reports, case series or pilot studies; thus, a cautiousapproach is warranted until further evidence-based support is pro-vided.

2. Incidence, mechanisms, and physiopathology

It is difficult to establish true figures regarding the incidence,mortality, and morbidity of IP because of the tendency to under-report complications.

The incidence of perforation in diagnostic gastroscopy is around0.03% with a mortality rate of 17% and a morbidity rate of 40% [2,3].When interventional procedures are included, this ratio rangesbetween 0.5 and 5% in EMR [4,5], 4 and 4.8% in ESD [5,6], whileit reaches 2.2% in esophageal dilation [7].

As for colonoscopy, the perforation rate varies between 0.03 and3% and involves mainly the sigmoid colon. Morbidity and mortal-ity are approximately 36% and 7% respectively [8–11]. In colorectalEMR, IP is reported to occur in 0.2–0.91% and ESD carries a perfo-

ration risk of 3.3–5.7% [9,12], with a very low mortality rate.

In endoscopic retrograde cholangiopancreatography (ERCP),perforation occurs in 0.35–2% and carries a mortality rate of 16–18%[13–16].

Ltd. All rights reserved.

Page 2: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

1 and Li

c(

ts(t

2

tiu

morrii

tsaul

tden[2dgtI

2

tos[

2

tmctlccmbe[uta

96 N. Al Ghossaini et al. / Digestive

Finally, endoscopic ultrasound (EUS) is a relatively safe pro-edure with a perforation rate of 0.03% and a low mortality rate<0.01%) [17,18].

The mechanism of gastrointestinal perforation is mainly relatedo three factors: mechanical trauma resulting from excessive pres-ure applied by the endoscope or the endoscopic instrumentbougies, balloon, guidewire, biopsy forceps), direct resection ofhe muscularis propria, and thermal necrosis [11,19].

.1. Mechanical trauma

In the esophagus, iatrogenic mechanical trauma can be poten-iated by the presence of stricture, severe inflammation, tumor,mpacted food and anatomical abnormality like Zenker’s divertic-lum [3].

Esophageal dilation consists in stretching or splitting theucosa and the underlying circular muscle. Balloon dilation exerts

nly a radial force; hence, the more it is inflated the higher theisk of perforation. On the other hand, bougie dilation exerts bothadial and axial forces, therefore, risk factors for IP related to its usenclude its diameter, the angle of taper, the surface friction, and thentrinsic characteristics of the stricture [20].

As for the colon, predisposing factors for IP include fragility ofhe colonic wall as a result of active inflammation, pelvic adhe-ions secondary to previous pelvic surgery, poor bowel preparation,dvanced patient age, female sex, multiple comorbidities, divertic-losis, and forceful advancement of the endoscope through bowel

oops [21].In endoscopic retrograde cholangiopancreatography (ERCP),

hree main types of perforation have been described. Kim et al.ivide these perforations into type 1, when they are induced by thendoscope before approaching the papilla, type 2, secondary to can-ulation of the papilla, and type 3, when induced by the guidewire22]. Perforations related to ampullectomy can be included in type. The main risk factors for IP include nondilated common bileuct, duration of the procedure, dilatation of biliary stricture, agereater than 65 years, intra-diverticular papilla, submucosal con-rast medium injection, personal history of ERCP, previous BillrothI procedure, and duodenal stenosis [13–16].

.2. Direct bowel resection

Direct bowel resection is most often related to inappropriateissue gripping with the polypectomy snare (inadvertent capturef normal adjacent mucosa within the snare loop) or to deep dis-ection of the bowel wall layers, causing a breach into the serosa19].

.3. Thermal injury

During polypectomy, when the electrical current extends pasthe mucosa into the muscularis propria and serosa, a trans-

ural burn may take place leading to serosal necrosis. Thisan happen during the removal of large polyps, which requirehe use of prolonged intensive thermal energy. Likewise, pro-onged application of the heater probe on the wall, unadaptedhoice of electrosurgical mode during polypectomy, and directontact of Argon plasma coagulation (APC) with the mucosa,ay lead to IP [11,19,23]. Other rare complications have also

een described with APC; namely, gas explosion in the pres-nce of combustible gases (oxygen, hydrogen, and methane)

24], and unintended remote burning via the electric arc whensing APC near a metallic stent or clip [25]. Special atten-ion should be paid when applying APC during EMR, ESD, ormpullectomy.

ver Disease 46 (2014) 195–203

3. Therapeutic means

Shifting insufflation to carbon dioxide (CO2), instead of air, hasbeen shown to benefit in decreasing abdominal pain and discom-fort after colonoscopy [26]. It also helps to reduce postproceduralmediastinal emphysema in patients undergoing esophageal ESD,since the esophagus is devoid of serosa [27]. Advantages of usingcarbon dioxide insufflation have also been demonstrated in pro-longed upper gastrointestinal procedures, and when perforation isdiscovered during therapeutic endoscopy, in which case, shiftinginsufflation from air to carbon dioxide can be very helpful [28].

In some cases of severe abdominal distension, transcutaneousneedle decompression has been suggested to avoid tension pneu-moperitoneum [5]. Staying as close as possible to the perforationsite is important so that endoscopic accuracy is optimal.

Some authors recommend injecting diluted indigo carmine intothe submucosa during EMR and ESD. If the resection base is blue,the submucosa is intact; if it is white, this means that the muscularispropria has been reached. Larger perforations secondary to blunttrauma may appear as a tear in the wall with rapid development oftension pneumoperitoneum [19].

3.1. Primary repair

Many tools have been used in the endoscopic closure of IP. Thefollowing are the most frequently described.

3.1.1. ClipsClips were initially designed for hemostasis and marking. Their

use was then extended to the closure of IP in gastrointestinalendoscopy. They seem to provide adequate apposition of mucosaand submucosa; however, their action on the muscularis propriaand serosa is rarely obtained because of their relatively superficialeffect [1].

There are several types of clips available on the market [29]:loadable and preloaded, directional and non-directional, recap-turable and nonrecapturable, triple-jawed and double-jawed; inaddition, there are different jaw opening widths according to themanufacturer.

A specific type, the over-the-scope-clip (OTSC) (OvescoEndoscopy, Tübingen, Germany), is loadable at the end of an endo-scope with a cap. It is releasable by a technique using a thread and aspool, resembling band ligation [30]. The two edges of the perfora-tion can be simply suctioned inside the cap, or gripped with a TwinGrasper, a forceps whose jaws are able to move independently [31].This type of clips was reported to provide more strength and bettertissue capture [30].

3.1.2. Sutures (endoscopic stitching)They were initially described in the closure of gastric openings

made during NOTES. Some of them provide an efficacy compa-rable with that of handmade surgical sutures, but they are quitedifficult to use. Many types have been described in the literature[32,33]. The T-Tags (Ethicon Endosurgery, Cincinnati, OH, USA)use T-shaped anchors, placed transmurally and tied together inpairs. The Purse String Modified T-Tags (Cook Endoscopy, Winston-Salem, NC, USA) consist in deploying T-Tags with a small metalloop around the perforation. Loops are then pulled so that a pursestring closure is obtained. The Eagle Claw VIII (Olympus Corpora-tion, Tokyo, Japan) is an over-the-scope device, fixing one woundedge with a jaw, while a curved needle, situated on the otherjaw, penetrates the opposite edge and delivers the suture. The

Purse String Suturing Device (LSI Solution, Victor, NY, USA) usessuction to approximate wound edges and then deploys titaniumknots in a purse string fashion. The Flexible Endostitch (Covidien,North Haven, CT, USA) holds a sharp needle that creates a running
Page 3: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

and Li

sfitbtdPb

3

UbebTut

3

Tabtoe

3

oecesn

tb

3

ecetcc

4s

tcnb

4

aE

N. Al Ghossaini et al. / Digestive

uture through the defect. The Plicator (NDO Surgical Inc., Mans-eld, MA, USA) is an endoscopic tool initially designed for treatinghe gastro-esophageal reflux disease. It delivers transmural sutureundles to close the IP. The Overstitch Endoscopic Suturing Sys-em (Apollo Endosurgery, Austin, TX, USA) is a single-use suturingevice requiring a double channel therapeutic endoscope. The G-rox needle (USGI, San Capistrano, CA, USA) has promising results,ut tests in vivo are still pending.

.1.3. StaplesPower Stapler (Power Medical Interventions, Langhorne, PA,

SA) is an endoscopic tool consisting of a stapler with a flexi-le extremity that measures 75 mm × 17 mm. It was assessed inxperimental studies on animals with initial encouraging results,ut it is not marketed anymore because of technical difficulties.hese difficulties are related to its introduction over a guidewirender endoscopic guidance and the complexity of its handling inhe digestive tract [34–36].

.1.4. Biological glueThe most commonly used biological glues are based on fibrin.

hey combine fibrinogen and thrombin to form an acellular clotnd have tissue-healing properties. They are completely absorbedy macrophages and fibroblasts within a fortnight [37,38]. Anotherype of sealing based on cyanoacrylate has been described. The usef biological glue can be considered in the treatment of chronicsophageal perforations or postsurgical fistulas [39].

.2. Diversion with stent

This technique is mainly applied to the esophagus becausef its anatomical conformation. Stent deployment following anndoscopic IP helps to cover the parietal defect, preventingontamination of surrounding tissues. Its placement promotes re-pithelialization and allows rapid resumption of oral nutrition. Thetent must be covered, thus removable if the underlying tissue isot malignant.

There are several types of esophageal stents: metallic (par-ially or completely covered), plastic (covered, expandable), andiodegradable.

.3. Endoscopic vacuum-assisted closure (EVAC)

This method has been described in the treatment of chronicsophageal perforations and in postsurgical esophageal leaks. Itonsists in placing a nasogastric tube in the necrotic cavity, underndoscopic guidance, after a foam sponge has been attached to itsip. A continuous negative pressure is applied so as to promoteollapse of the fistula until the wound heals. The sponge must behanged twice a week [40].

. Suggested closure method for different gastrointestinalegments

The following methods have been described in the literatureo close IP endoscopically; however, most of them are based onase series and animal studies. Further large prospective trials areeeded to evaluate safety, ease of use, cost effectiveness, and riskenefit of these procedures.

.1. Esophagus

Endoscopic closure is of particular importance in the man-gement of IP located in the thoracic and abdominal esophagus.ndoscopic treatment is more difficult in the cervical esophagus as

ver Disease 46 (2014) 195–203 197

stents are often poorly tolerated and the unstable position preventsthe achievement of a direct closure [41,42].

If IP happens in achalasia, resectable tumor, caustic stenosis, orin very large perforations (>2 cm), surgical treatment is proposed[43]. In healthy esophagus, inoperable patients, and unresectabletumor, endoscopic treatment may be attempted [44].

The use of clips applies for small perforations [1,44–46]. Endo-clips have an excellent technical success rate and a good clinicaloutcome.

In those who develop large esophageal perforation (>1.5 cm),treatment with completely covered self-expandable metallic stents(SEMS) or self-expandable plastic stents (SEPS) can be considered[41,43,47,48].

In the proximal esophagus, SEPS or ultraflexible SEMS seem toprovide a lesser degree of foreign body sensation while completelycovered Nitinol stents are used in most distal perforations. The stentmust be positioned so that it covers 3–5 cm above and below theperforation. Just before stenting, some authors propose the place-ment of a gastrostomy tube to ensure gastric drainage in the first48 h and enteral nutrition thereafter. Insertion of a naso-jejunaltube may also be useful [41,49].

After endoscopic treatment, a computed tomography (CT) scanis essential to detect any possible mediastinal collection. If the scanis normal or if it reveals a pneumomediastinum without collectionof fluids (contained perforation), antibiotics should be prescribedfor 14 days [41]. A liquid diet can be allowed 48 h after the repaironly if radiological tests using a water-soluble contrast mediumshow no leakage. If a mediastinal or pleural collection is noticed(uncontained perforation), concomitant surgical or radiologicaldrainage is mandatory since the closure of the perforation preventstheir internal drainage. Appropriate external drainage can be car-ried out using thoracoscopy, thoracotomy, placement of a chesttube, or even by neck surgery [43]. In this case, broad-spectrumantibiotics are advisable (e.g., tazobactam 4 g/8 h), some authorsrecommend adding antifungals. Chest X-ray is to be repeated every2 days to verify the absence of stent migration. A gastroscopy is pro-posed at 4 weeks to examine the site of perforation and replace orreposition the stent if needed [50]. The average length of stay inhospital varies between 18 and 44 days. The stent migration rate is20–30% [41,49], in which case, the perforation is left uncovered.

The OTSC has also been described in closing esophageal perfo-rations with very good results [51].

An algorithm for the management of these perforations is sug-gested in Fig. 1.

4.2. Stomach

Two methods of endoscopic closure with endoclips have beendescribed by Minami et al.: the single closure method, and theomental patch method [5].

While the former is used for linear perforations measuring lessthan 1 cm, a size that corresponds to the opening width of a clip,the latter helps to repair larger perforations (>1 cm) and consists inusing the greater or lesser omentum, suctioned into the perforationto form a patch that is held in place by the application of multipleclips. During the endoscopic closure, abdominal palpation must beperformed regularly. If significant bloating is noticed, decompres-sion of the peritoneal cavity has to be performed using a 14-gaugecatheter, after a test with a 23-gauge needle syringe filled withsaline solution. Decompression of the pneumoperitoneum helps toavoid postoperative pain, peritonitis, abscess formation, and neu-

rogenic shock. Patients are often kept in hospital for observationfor 4–7 days; they are put on broad spectrum antibiotic therapy,pain killers, and proton pump inhibitors (PPI). They remain fastingfor 48 h with a nasogastric tube in place for aspiration.
Page 4: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

198 N. Al Ghossaini et al. / Digestive and Liver Disease 46 (2014) 195–203

mana

sroamo

t

4

mEt[fptms

tonitis requires immediate surgical care [13,57].Type 1 perforations (before approaching the papilla) are usually

closed surgically. Endoscopic treatment with clips can be offered if

Fig. 1. Suggested algorithm for the

A recent pilot study evaluated the use of a synthetic omentumubstitute made of self-expandable foam matrix (polyurethane) forepairing gastric IP in pigs. The clinical outcome was comparable tomental patch, but migration and inadequate sealing was a concernnd further development is needed before its use can be recom-ended [52]. Using OTSC permits the closure of gastric perforations

f up to 2 cm with adequate tightness [30,31].A suggested algorithm for the management of gastric perfora-

ions is represented in Fig. 2.

.3. Duodenum, periampullary region, and bile ducts

Some studies evaluated the incidence of post-ERCP pneu-operitoneum by performing a routine abdominal CT scan after

RCP. They found a pneumoperitoneum in up to 29% of asymp-omatic patients who underwent uncomplicated interventions53,54]. Consequently, conservative non-surgical treatment of per-oration occurring after ERCP is possible despite the presence of a

neumoperitoneum, given that the patient has few or no symp-oms. However, if abdominal pain, fever, or sepsis appears, surgery

ust be considered, since a delayed intervention could lead toevere morbidity and mortality [15,55,56].

gement of esophageal perforation.

Immediate diagnosis of periampullary perforation and its treat-ment by both duodenal and biliary drainage (nasobiliary andnasogastric drain) in addition to broad-spectrum antibiotics canlead to healing without surgical treatment in about 80% of patients.However, the presence of retroperitoneal fluid collection or peri-

Fig. 2. Suggested algorithm for the management of gastric perforation.

Page 5: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

N. Al Ghossaini et al. / Digestive and Liver Disease 46 (2014) 195–203 199

e man

t[

tisao

atooatacf

d1

sEtTu

r

idtbmpar

Fig. 3. Suggested algorithm for th

hey are detected immediately, and if their size is less than 15 mm15].

Several methods of clipping are described: the easiest way iso place one or more endoclips in a linear fashion. This methods proposed for small perforations that are easily accessible. Closeupervision is required and an abdominal CT scan at 48 h is advis-ble in order to control the progression. Reoperation in the eventf clinical deterioration should be promptly considered [1].

Another method, described in larger perforations (10–13 mm)nd/or those located at angulations, requires an endoscope with aransparent cap to facilitate the unfolding of the mucosa, reductionf angulations, and suction of the perforation site for better grippingf the clip. Antibiotics, parenteral nutrition and PPIs are routinelydministered. Patients are authorized to eat starting from the 4tho 8th day, after a CT scan reveals the absence of further leakagend a small bowel series shows no extravasation of water-solubleontrast medium. The duration of hospitalization is reported to varyrom 10 to 27 days [58,59].

There are only a few reports describing the use of OTSC in theuodenum, but it appears to be efficient for perforations less than5 mm in diameter [30,60–62].

A recent paper describes a technique called “clutching rosetems” to close a perforation in the second duodenum after EMR.ndoclips are placed around the perimeter of the wound edges andhey are brought together using a snare. Fibrin glue is then applied.his procedure was previously described for colonic perforationsnder the name of the “tulip bundle technique” [63].

Type 2 perforation (secondary to cannulation of the papilla)equires more complex management.

If the diagnosis is made during the endoscopic procedure, thensertion of either a fully covered metallic stent, or a nasobiliaryrain and a nasogastric tube for suction is possible. A CT scan ofhe abdomen and pelvis is then performed to search for a possi-le retroperitoneal collection, which is an indication for surgical

anagement. Otherwise, using broad spectrum antibiotics with the

atient fasting, and diverting bile and gastrointestinal secretionsppear to be effective in the majority of cases. Close monitoring isecommended for at least 48 h and a surgical consultation should

agement of duodenal perforation.

be obtained [22,64]. Some authors have described the closure ofthe IP site using hemostatic clips. Special attention should be paidto avoid the biliary and pancreatic ducts. That is why clips must bereleased onto the upper part of the sphincterotomy orifice. Insert-ing a naso-biliary drain is advisable in this case [65,66].

If a type 2 perforation is discovered after the end of the proce-dure, a CT scan of the abdomen and pelvis with administration ofwater-soluble oral contrast medium should be performed. Surgeryis decided upon if there is a significant extravasation of contrastmedium or a retroperitoneal collection. If only a pneumoperi-toneum is revealed, clinical monitoring with antibiotics, fasting,and nasogastric suctioning can be considered an alternative tosurgery. At 24 h, the clinical course can guide the decision [22].

A score was developed to help decide whether patients shouldbe sent for surgery or closely monitored under conservative treat-ment. One point was assigned for each of the following items: fever,tachycardia, leukocytosis, and abdominal guarding. Patients withscores 3 and 4 have all been operated upon. However, this score isto be heeded with great caution because it is a retrospective studylimited to 32 perforations [15].

Type 3 perforations (induced by the guidewire) are often lessaggressive and require nasobiliary drainage or close monitoringwith antibiotic administration [22,57,64].

Based on several case series, duodenal perforations can be man-aged as illustrated in Fig. 3.

4.4. Colon

The surgical team must be notified for each colonic IP, evenif endoscopic closure is performed. Broad-spectrum antibioticsand intravenous hydration are to be initiated. Patients should beregularly examined for any peritoneal irritation. A radiologicalexamination such as plain abdominal radiography or CT must beperformed immediately after endoscopic closure and 48 h later. The

patient must fast until disappearance of pain and fever, resump-tion of bowel movement, return of appetite, and normalization ofinflammatory parameters (CRP and WBC). If an aggravation occurs,surgical treatment is indicated [19].
Page 6: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

200 N. Al Ghossaini et al. / Digestive and Liver Disease 46 (2014) 195–203

e ma

iScSae2a1atdtp[

iTsmpttvod

mp

cta[p

rs

Fig. 4. Suggested algorithm for th

The use of endoclips to close colonic IP has a technical successn 69–100% of cases and clinical success in 51–89.6% [1,67–69].ubsequent surgical treatment has been reported in 7.4–24% ofases because of clinical deterioration or abscess formation [68,70].everal conditions must be met to attempt this type of closure:

perforation size less than 1 cm, a clean colonic content and anxperienced endoscopic gastroenterology team. Within the first4 h, risk factors that predict unfavorable clinical outcome include

perforation resulting from diagnostic colonoscopy or larger than0 mm, leukocytosis > 10,000 mm3, temperature ≥ 37 ◦C, severebdominal pain requiring narcotic analgesics, large pneumoperi-oneum (≥3 cm between the upper liver margin and the rightiaphragm on plain chest X-ray) [70,71]. CO2 insufflation is impor-ant since it helps to maintain the hemodynamic stability of theatient and prevents the appearance of early peritoneal irritation26,72].

The technique consists in opening the clip, then pulling it untilts jaws are in contact with the distal extremity of the endoscope.his allows the endoscope and the clip to be moved together as aingle block. Then, rotation is performed so that the jaws of the clipake a 90-degree-angle with the perforation axis. One jaw is lightly

ushed onto the edge of the perforation and suction is made in ordero obtain the maximum amount of tissue between the two jaws ofhe clip, which is released immediately. It is preferable to closeertical perforations from the top down, horizontal and circularnes from left to right. Note that the first clip is usually the mostifficult to place [19].

If the perforation occurs during an ESD, some authors recom-end finishing the procedure before placing a clip since it might

revent endoscopic resection of the lesion thereafter [19].Closure of colonic IP with clips decreases the risk of peritoneal

ontamination, prevents adhesions secondary to surgery, reduceshe hospital stay (lower risk of post-operative ileus), and helps tovoid general anesthesia if endoscopy is performed under sedation73]. OTSC has also been reported to be efficient in closing colon

erforations [30,62].

Four innovative methods have been described, but their useemains anecdotal. The first one requires a dual channel endo-cope and uses several clips and one endoloop. The endoloop is

nagement of colonic perforation.

fixed with clips onto the edges of the perforation before it istightened [74]. The second method uses a single working channelendoscope and a combination of endoloop–clips–glue (tulip bundletechnique). Clips are positioned on the perforation edges, then, theyare tightened with an endoloop, and glue is applied to their basesto complete the closure [75]. The third method requires a doublemetal ring called the “8-ring.” This ring is attached with a clip toeach edge of the perforation. This procedure helps to draw the edgestogether, then, consolidation can be performed by the deploymentof additional clips [76]. The fourth method uses an OTSC and endo-clips; it is performed by inducing a therapeutic intussusception ofan epiploic appendix with aspiration. This procedure requires thecomplete removal of the colonoscope in order to mount the deviceon its distal end prior to its reinsertion [72].

Fig. 4 reviews the different methods used to treat colonic perfo-ration, as described in the literature.

5. Discussion

Most data about the endoscopic closure of IP are case reports andsmall retrospective series with a bias toward publishing technicallysuccessful cases. Very rarely, prospective studies are conducted onanimals, but they include a small number of individuals (pilot stud-ies). Since it is very difficult to carry out controlled trials to comparesurgical and endoscopic management, the latter can be consideredin selected cases, provided strict rules are followed.

Two entities must be differentiated: acute and chronic IP.Acute perforation is an emergency that requires prompt closureto prevent visceral space contamination. Closure can be attemptedendoscopically if no contamination occurred or if the patient isinoperable, while surgery is considered in the other cases. ChronicIPs are usually complicated by fistulas and abscesses and oftenrequire surgical treatment. Endoscopic treatment including glue,stents, endoclips, OTSC, and EVAC may be considered as adjunctiveor alternative to surgery.

While hemoclip closure is technically successful in around 91%of cases, clinical success varies between 59 and 100% of cases[68,70]. Furthermore, several limitations should be underlined;particularly, the difficulty in evaluating the complete closure of the

Page 7: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

and Li

Ivlsawmrnio[cbwporetpihaeo

scmop

eoaboocsmaolsfiLg

mgwcrh

6

seas

[

[

[

N. Al Ghossaini et al. / Digestive

P related to early detachment of clips or to their inability to pro-ide perfect sealing of the perforation site [72]. Minor leaks canead to delayed peritonitis or abscess formation. In these cases,urgery is performed beyond the optimal period and is often moreggressive, leading sometimes to colon resection and to diversionith colonostomy [70]. Another drawback is that endoscopic treat-ent requires the prolongation of the procedure, which usually

esults in a larger pneumoperitoneum and in greater abdomi-al distension. Consequently, some authors advise shifting to CO2

nsufflation or performing transcutaneous needle decompressionf the pneumoperitoneum if endoscopic treatment is decided upon5]. Moreover, the use of endoclips may render further laparoscopiclosure technically difficult [70]. As for OTSC, technical success haseen reported in up to 91–93% and clinical success in 89% [62,77,78]ith the advantage of providing a full thickness closure and a com-arable efficiency to manual surgical suture [72]. However, the usef the Twin Grasper is sometimes difficult, especially in positionsequiring retroflexion (gastric fundus) and when wound edges areverted, in which case, aspiration might be used to approximatehe edges [77]. The main drawback of OTSC is the necessity to com-letely withdraw the endoscope in order to mount the device onto

ts distal extremity. On the other hand, while the retention period ofemoclips is an average of 1–4 weeks [79], that of OTSC is unknownnd seems much longer [78,80]. Some cases of clips remainingmbedded in the mucosa for several months because of the devel-pment of granulation tissue have been reported [72,80,81].

Regarding suturing devices, efficacy seems to be comparable tourgical suturing, but their use is complicated and requires spe-ial technical skills. Furthermore, they are not readily available andany of them are prototypes used in experimental animal studies

r in NOTES. In the future, simpler suturing kits may be developedermitting a more widespread use.

Finally, covered stents have been used in the treatment ofsophageal and duodenal perforations. They should be removedr replaced within 8 weeks; otherwise, the inner coat may be dam-ged, preventing further removal. These stents are likely to migrateecause of the absence of stenosis in most IPs [82]. Stent migrationccurs in around one third of cases [83]. The use of clips placedn their proximal edges may prevent them from migrating. Thislipping of the proximal ending has high technical and clinicaluccess rates (100% and 88% respectively), significantly reducingigration rate (0 to 13%) [83,84]. The mechanism of action of clip

nchoring may be the prevention of early stent migration sec-ndary to peristalsis awaiting complete stent expansion 24–48 hater [83]. Vanbiervliet et al. showed, through multivariate analy-is, that clipping of the covered stent was the unique independentactor preventing migration, while there was no influence regard-ng stent diameter or its localization in the gastrointestinal tract.onger stents and gap closing stents (perforation, fistula, and sur-ical disunion) seemed to have a lower risk of migration [83].

Different stent modifications have been attempted to preventigration (flip-flop ring at the proximal end [85], external antimi-

ration struts [86,87], double-layering [88], fixation to the earlobeith either a silk thread [89] or a polypectomy snare [90], per-

utaneous cervical pexy under ultrasound guidance [50]), but theesults were disappointing, with a migration rate that remainedigh (20–40%).

. Conclusion

Iatrogenic perforations are serious complications that are pos-

ible to manage endoscopically in certain circumstances. Extensivendoscopic knowledge, a highly trained endoscopy team, and thevailability of adapted equipments are required to ensure safe clo-ure of the perforation. Moreover, close collaboration with the

[

[

ver Disease 46 (2014) 195–203 201

surgical team is emphasized, even after a successful endoscopicrepair.

In the esophagus, immediate identification of the perfora-tion site and stable hemodynamics are necessary conditions forattempting endoscopic repair. If the perforation is contained,endoscopic management and wide spectrum antibiotics may besufficient. When there is uncontained perforation, concomitantradiological or surgical drainage of the collection is necessary. Inthe stomach, the main criterion is the size of the perforation. In theduodenum, the size of the perforation and the presence of extralu-minal fluid collection help to determine the type of management. Inthe colon, well-prepared bowel, a hemodynamically stable patient,the reasonable size of the perforation, and excellent postprocedu-ral monitoring are fundamental for proceeding with endoscopicclosure.

Hemoclips are preferred in small perforations because they arereadily available and easy to use. In larger perforations, the use ofOTSC, a combination of hemoclips with loops, glue, and rings or theuse of a stent can be considered. Forty-eight to 72 h later, imagingwith administration of oral contrast medium should be performedto make sure that there is no leakage before allowing the resump-tion of oral feeding. Drainage of any collections, administration ofantibiotics, and nutritional support are essential adjuncts. Last butnot least, the surgical team must be systematically notified even ifendoscopic management is achieved without complication, so thatsurgery is promptly performed if there is subsequent deteriorationin the general condition of the patient.

Conflict of interest statement

We certify that there is no conflict of interest with any financialorganization regarding the material discussed in the manuscript.

References

[1] Mangiavillano B, Viaggi P, Masci E. Endoscopic closure of acute iatrogenic per-forations during diagnostic and therapeutic endoscopy in the gastrointestinaltract using metallic clips: a literature review. Journal of Digestive Diseases2010;11:12–8.

[2] Eisen GM, Baron TH, Dominitz JA, et al. Complications of upper GI endoscopy.Gastrointestinal Endoscopy 2002;55:784–93.

[3] Merchea A, Cullinane DC, Sawyer MD, et al. Esophagogastroduodenoscopy-associated gastrointestinal perforations: a single-center experience. Surgery2010;148:876–80.

[4] Kojima T, Parra-Blanco A, Takahashi H, et al. Outcome of endoscopic mucosalresection for early gastric cancer: review of the Japanese literature. Gastroin-testinal Endoscopy 1998;48:550–4.

[5] Minami S, Gotoda T, Ono H, et al. Complete endoscopic closure of gas-tric perforation induced by endoscopic resection of early gastric cancerusing endoclips can prevent surgery (with video). Gastrointestinal Endoscopy2006;63:596–601.

[6] Oda I, Gotoda T, Hamanaka H. Endoscopic submucosal dissection for early gas-tric cancer: technical feasibility, operation time and complications from a largeconsecutive series. Digestive Endoscopy 2005;17:54–8.

[7] Fry LC, Monkemuller K, Neumann H, et al. Incidence, clinical management andoutcomes of esophageal perforations after endoscopic dilatation. Zeitschrift furGastroenterologie 2007;45:1180–4.

[8] Dominitz JA, Eisen GM, Baron TH, et al. Complications of colonoscopy. Gastroin-testinal Endoscopy 2003;57:441–5.

[9] Iqbal CW, Cullinane DC, Schiller HJ, et al. Surgical management and outcomesof 165 colonoscopic perforations from a single institution. Archives of Surgery2008;143:701–6.

10] Luning TH, Keemers-Gels ME, Barendregt WB, et al. Colonoscopic perforations:a review of 30,366 patients. Surgical Endoscopy 2007;21:994–7.

11] Panteris V, Haringsma J, Kuipers EJ. Colonoscopy perforation rate, mecha-nisms and outcome: from diagnostic to therapeutic colonoscopy. Endoscopy2009;41:941–51.

12] Oka S, Tanaka S, Kanao H, et al. Current status in the occurrence of postoper-ative bleeding, perforation and residual/local recurrence during colonoscopic

treatment in Japan. Digestive Endoscopy 2010;22:376–80.

13] Enns R, Eloubeidi MA, Mergener K, et al. ERCP-related perforations: risk factorsand management. Endoscopy 2002;34:293–8.

14] Freeman ML, Nelson DB, Sherman S, et al. Complications of endoscopic biliarysphincterotomy. New England Journal of Medicine 1996;335:909–18.

Page 8: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

2 and Li

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

02 N. Al Ghossaini et al. / Digestive

15] Knudson K, Raeburn CD, McIntyre Jr RC, et al. Management of duodenal andpancreaticobiliary perforations associated with periampullary endoscopic pro-cedures. American Journal of Surgery 2008;196:975–81.

16] Loperfido S, Angelini G, Benedetti G, et al. Major early complications from diag-nostic and therapeutic ERCP: a prospective multicenter study. GastrointestinalEndoscopy 1998;48:1–10.

17] Bournet B, Migueres I, Delacroix M, et al. Early morbidity of endoscopic ultra-sound: 13 years’ experience at a referral center. Endoscopy 2006;38:349–54.

18] Rathod V, Maydeo A. How safe is endoscopic ultrasound? A retrospectiveanalysis of complications encountered during diagnosis and interventionalendosonography in a large individual series of 3006 patients from India. Gas-trointestinal Endoscopy 2002;56 [Abstract].

19] Raju GS, Saito Y, Matsuda T, et al. Endoscopic management of colonoscopicperforations (with videos). Gastrointestinal Endoscopy 2011;74:1380–8.

20] Pasha SF, Fleischer DE. In: Classen M, Tytgat GNJ, Lightdale CJ, editors. Dilationtechniques. 2010. p. 323–30.

21] Lohsiriwat V. Colonoscopic perforation: incidence, risk factors, managementand outcome. World Journal of Gastroenterology 2010;16:425–30.

22] Kim BS, Kim IG, Ryu BY, et al. Management of endoscopic retrogradecholangiopancreatography-related perforations. Journal of the Korean SurgicalSociety 2011;81:195–204.

23] Chuang CH, Chou TC, Chen CY. Minute perforation after argon plasma coag-ulation for management of small colonic polyps. Endoscopy 2009;41(Suppl.2):E251–2.

24] Ben SE, Mathieu N, Roque I, et al. Bowel explosion with colonic perforationduring argon plasma coagulation for hemorrhagic radiation-induced proctitis.Gastrointestinal Endoscopy 2003;57:412–3.

25] Chen YK, Jakribettuu V, Springer EW, et al. Safety and efficacy of argon plasmacoagulation trimming of malpositioned and migrated biliary metal stents: acontrolled study in the porcine model. American Journal of Gastroenterology2006;101:2025–30.

26] Wang WL, Wu ZH, Sun Q, et al. Meta-analysis: the use of carbon dioxideinsufflation vs room air insufflation for gastrointestinal endoscopy. AlimentaryPharmacology and Therapeutics 2012;35:1145–54.

27] Maeda Y, Hirasawa D, Fujita N, et al. A pilot study to assess mediastinal emphy-sema after esophageal endoscopic submucosal dissection with carbon dioxideinsufflation. Endoscopy 2012;44:565–71.

28] Sagawa T, Kakizaki S, Iizuka H, et al. Analysis of colonoscopic perforationsat a local clinic and a tertiary hospital. World Journal of Gastroenterology2012;18:4898–904.

29] Coumaros D, Mavrogenis G, Lakhrib N. Gestion immédiate de la perforation enendoscopie. Acta Endoscopica 2010;40:332–6.

30] Parodi A, Repici A, Pedroni A, et al. Endoscopic management of GI perfora-tions with a new over-the-scope clip device (with videos). GastrointestinalEndoscopy 2010;72:881–6.

31] Zhang XL, Qu JH, Sun G, et al. Feasibility study of secure closure of gastric fundusperforation using over-the-scope clips in a dog model. Journal of Gastroenterol-ogy and Hepatology 2012;27:1200–4.

32] Banerjee S, Barth BA, Bhat YM, et al. Endoscopic closure devices. Gastrointesti-nal Endoscopy 2012;76:244–51.

33] Raju GS. Endoscopic closure of gastrointestinal leaks. American Journal of Gas-troenterology 2009;104:1315–20.

34] Arezzo A, Morino M. Endoscopic closure of gastric access in perspectiveNOTES: an update on techniques and technologies. Surgical Endoscopy2010;24:298–303.

35] Kaehler G, Grobholz R, Langner C, et al. A new technique of endoscopic full-thickness resection using a flexible stapler. Endoscopy 2006;38:86–9.

36] Magno P, Giday SA, Dray X, et al. A new stapler-based full-thickness trans-gastric access closure: results from an animal pilot trial. Endoscopy 2007;39:876–80.

37] Becker JC, Beckbauer M, Domschke W, et al. Fibrin glue, healing of gastricmucosal injury, and expression of growth factors: results from a human in vivostudy. Gastrointestinal Endoscopy 2005;61:560–7.

38] Jackson MR. Fibrin sealants in surgical practice: an overview. American Journalof Surgery 2001;182(Suppl. 2):1S–7S.

39] Lee YC, Na HG, Suh JH, et al. Three cases of fistulae arising from gastroin-testinal tract treated with endoscopic injection of Histoacryl. Endoscopy2001;33:184–6.

40] Brangewitz M, Voigtlander T, Helfritz FA, et al. Endoscopic closure of esophagealintrathoracic leaks: stent versus endoscopic vacuum-assisted closure, a retro-spective analysis. Endoscopy 2013;45:433–8.

41] D‘Cunha J, Rueth NM, Groth SS, et al. Esophageal stents for anastomoticleaks and perforations. Journal of Thoracic and Cardiovascular Surgery2011;142:39–46.

42] Freeman RK, Ascioti AJ. Esophageal stent placement for the treatment of per-foration, fistula, or anastomotic leak. Seminars in Thoracic and CardiovascularSurgery 2011;23:154–8.

43] Eroglu A, Turkyilmaz A, Aydin Y, et al. Current management of esophagealperforation: 20 years experience. Diseases of the Esophagus 2009;22:374–80.

44] Raju GS, Thompson C, Zwischenberger JB. Emerging endoscopic options inthe management of esophageal leaks (videos). Gastrointestinal Endoscopy

2005;62:278–86.

45] Qadeer MA, Dumot JA, Vargo JJ, et al. Endoscopic clips for closing esophagealperforations: case report and pooled analysis. Gastrointestinal Endoscopy2007;66:605–11.

[

ver Disease 46 (2014) 195–203

46] Siersema PD. Treatment of esophageal perforations and anastomotic leaks:the endoscopist is stepping into the arena. Gastrointestinal Endoscopy2005;61:897–900.

47] Gelbmann CM, Ratiu NL, Rath HC, et al. Use of self-expandable plastic stents forthe treatment of esophageal perforations and symptomatic anastomotic leaks.Endoscopy 2004;36:695–9.

48] Tuebergen D, Rijcken E, Mennigen R, et al. Treatment of thoracicesophageal anastomotic leaks and esophageal perforations with endolumi-nal stents: efficacy and current limitations. Journal of Gastrointestinal Surgery2008;12:1168–76.

49] Dai Y, Chopra SS, Steinbach M, et al. Esophageal stents for leaks andperforations. Seminars in Thoracic and Cardiovascular Surgery 2011;23:159–62.

50] Blackmon SH, Santora R, Schwarz P, et al. Utility of removable esophageal cov-ered self-expanding metal stents for leak and fistula management. Annals ofThoracic Surgery 2010;89:931–6.

51] Kirschniak A, Subotova N, Zieker D, et al. The Over-The-Scope Clip (OTSC) forthe treatment of gastrointestinal bleeding, perforations, and fistulas. SurgicalEndoscopy 2011;25:2901–5.

52] Bonin EA, Bingener J, Rajan E, et al. Omentum patch substitute for facilitat-ing endoscopic repair of GI perforations: an early laparoscopic pilot studywith a foam matrix plug (with video). Gastrointestinal Endoscopy 2013;77:123–30.

53] de Vries JH, Duijm LE, Dekker W, et al. CT before and after ERCP: detection ofpancreatic pseudotumor, asymptomatic retroperitoneal perforation, and duo-denal diverticulum. Gastrointestinal Endoscopy 1997;45:231–5.

54] Genzlinger JL, McPhee MS, Fisher JK, et al. Significance of retroperitoneal airafter endoscopic retrograde cholangiopancreatography with sphincterotomy.American Journal of Gastroenterology 1999;94:1267–70.

55] Avgerinos DV, Llaguna OH, Lo AY, et al. Management of endoscopic retrogradecholangiopancreatography: related duodenal perforations. Surgical Endoscopy2009;23:833–8.

56] Alfieri S, Rosa F, Cina C, et al. Management of duodeno-pancreato-biliary per-forations after ERCP: outcomes from an Italian tertiary referral center. SurgicalEndoscopy 2013;27:2005–12.

57] Stapfer M, Selby RR, Stain SC, et al. Management of duodenal perforation afterendoscopic retrograde cholangiopancreatography and sphincterotomy. Annalsof Surgery 2000;232:191–8.

58] Lee TH, Bang BW, Jeong JI, et al. Primary endoscopic approximation sutureunder cap-assisted endoscopy of an ERCP-induced duodenal perforation. WorldJournal of Gastroenterology 2010;16:2305–10.

59] Roses LL, Ramirez AG, Seco AL, et al. Clip closure of a duodenal perfo-ration secondary to a biliary stent. Gastrointestinal Endoscopy 2000;51:487–9.

60] Salord S, Gornals JB, Maisterra S, et al. Endoscopic closure of duodenal per-foration with an over-the-scope clip during endoscopic ultrasound-guidedcholangiopancreatography. Revista Espanola de Enfermedades Digestivas2012;104:489–90.

61] von Renteln D, Rudolph HU, Schmidt A, et al. Endoscopic closure of duodenalperforations by using an over-the-scope clip: a randomized, controlled porcinestudy. Gastrointestinal Endoscopy 2010;71:131–8.

62] Gubler C, Bauerfeind P. Endoscopic closure of iatrogenic gastrointestinal tractperforations with the over-the-scope clip. Digestion 2012;85:302–7.

63] Samarasena JB, Nakai Y, Park DH, et al. Endoscopic closure of an iatrogenicduodenal perforation: a novel technique using endoclips, endoloop, and fibringlue. Endoscopy 2012;44(Suppl. 2):E424–5. UCTN.

64] Wu HM, Dixon E, May GR, et al. Management of perforation after endoscopicretrograde cholangiopancreatography (ERCP): a population-based review. HPB(Oxford) 2006;8:393–9.

65] Katsinelos P, Paroutoglou G, Papaziogas B, et al. Treatment of a duodenal per-foration secondary to an endoscopic sphincterotomy with clips. World Journalof Gastroenterology 2005;11:6232–4.

66] Lee YS, Moon JH, Ko BM, et al. Endoscopic closure of a distal common bile ductperforation caused by papillary dilation with a large-diameter balloon (withvideo). Gastrointestinal Endoscopy 2010;72:616–8.

67] Heldwein W, Dollhopf M, Rosch T, et al. The Munich Polypectomy Study(MUPS): prospective analysis of complications and risk factors in 4000 colonicsnare polypectomies. Endoscopy 2005;37:1116–22.

68] Magdeburg R, Collet P, Post S, et al. Endoclipping of iatrogenic colonic perfora-tion to avoid surgery. Surgical Endoscopy 2008;22:1500–4.

69] Taku K, Sano Y, Fu KI, et al. Iatrogenic perforation at therapeutic colonoscopy:should the endoscopist attempt closure using endoclips or transfer immedi-ately to surgery? Endoscopy 2006;38:428.

70] Cho SB, Lee WS, Joo YE, et al. Therapeutic options for iatrogenic colon perfora-tion: feasibility of endoscopic clip closure and predictors of the need for earlysurgery. Surgical Endoscopy 2012;26:473–9.

71] Fujishiro M, Yahagi N, Kakushima N, et al. Successful nonsurgical managementof perforation complicating endoscopic submucosal dissection of gastrointesti-nal epithelial neoplasms. Endoscopy 2006;38:1001–6.

72] Diez-Redondo P, Blanco JI, Lorenzo-Pelayo S, et al. A novel system for endo-scopic closure of iatrogenic colon perforations using the Ovesco(R) clip and

omental patch. Revista Espanola de Enfermedades Digestivas 2012;104:550–2.

73] Raju GS, Ahmed I, Xiao SY, et al. Controlled trial of immediate endoluminalclosure of colon perforations in a porcine model by use of a novel clip device(with videos). Gastrointestinal Endoscopy 2006;64:989–97.

Page 9: Endoscopic treatment of iatrogenic gastrointestinal perforations: An overview

and Li

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[stent: its clinical usefulness for preventing stent migration. Endoscopy

N. Al Ghossaini et al. / Digestive

74] Matsuda T, Fujii T, Emura F, et al. Complete closure of a large defect after EMRof a lateral spreading colorectal tumor when using a two-channel colonoscope.Gastrointestinal Endoscopy 2004;60:836–8.

75] Mocciaro F, Curcio G, Tarantino I, et al. Tulip bundle technique and fibrin glueinjection: unusual treatment of colonic perforation. World Journal of Gastroen-terology 2011;17:1088–90.

76] Fujii T, Ono A, Fu KI. A novel endoscopic suturing technique using a speciallydesigned so-called “8-ring” in combination with resolution clips (with videos).Gastrointestinal Endoscopy 2007;66:1215–20.

77] Junquera F, Martinez-Bauer E, Miquel M, et al. OVESCO: a promising system forendoscopic closure of gastrointestinal tract perforations. Gastroenterologia yHepatologia 2011;34:568–72.

78] Voermans RP, Le Moine O, von RD, et al. Efficacy of endoscopic closure ofacute perforations of the gastrointestinal tract. Clinical Gastroenterology andHepatology 2012;10:603–8.

79] Shin EJ, Ko CW, Magno P, et al. Comparative study of endoscopic clips: dura-tion of attachment at the site of clip application. Gastrointestinal Endoscopy2007;66:757–61.

80] Law R, Irani S, Song LMWK, et al. Clip retention following endoscopicplacement of the Over-the-Scope Clip (OTSC). Gastrointestinal Endoscopy2013;77:AB221–2 [Abstract].

81] Iacopini F, Di LN, Altorio F, et al. Over-the-scope clip closure of two chronic

fistulas after gastric band penetration. World Journal of Gastroenterology2010;16:1665–9.

82] Choi HJ, Lee BI, Kim JJ, et al. The temporary placement of covered self-expandable metal stents to seal various gastrointestinal leaks after surgery.Gut and Liver 2013;7:112–5.

[

ver Disease 46 (2014) 195–203 203

83] Vanbiervliet G, Filippi J, Karimdjee BS, et al. The role of clips in preventingmigration of fully covered metallic esophageal stents: a pilot comparativestudy. Surgical Endoscopy 2012;26:53–9.

84] Kim ID, Kang DH, Choi CW, et al. Prevention of covered enteral stent migra-tion in patients with malignant gastric outlet obstruction: a pilot study ofanchoring with endoscopic clips. Scandinavian Journal of Gastroenterology2010;45:100–5.

85] Uitdehaag MJ, Siersema PD, Spaander MC, et al. A new fully covered stent withantimigration properties for the palliation of malignant dysphagia: a prospec-tive cohort study. Gastrointestinal Endoscopy 2010;71:600–5.

86] Ferreira LE, Baron TH, Wong Kee Song LM. Utility of a fully covered metal stentfor the treatment of benign esophageal conditions. Gastrointest Endoscopy2008;67:AB193 [Abstract].

87] Eloubeidi MA, Lopes TL. Novel removable internally fully covered self-expanding metal esophageal stent: feasibility, technique of removal, andtissue response in humans. American Journal of Gastroenterology 2009;104:1374–81.

88] Verschuur EM, Homs MY, Steyerberg EW, et al. A new esophageal stent design(Niti-S stent) for the prevention of migration: a prospective study in 42 patients.Gastrointestinal Endoscopy 2006;63:134–40.

89] Shim CS, Cho YD, Moon JH, et al. Fixation of a modified covered esophageal

2001;33:843–8.90] Manes G, Corsi F, Pallotta S, et al. Fixation of a covered self-expandable metal

stent by means of a polypectomy snare: an easy method to prevent stent migra-tion. Digestive and Liver Disease 2008;40:791–3.