: OPENING NEW EYES, SERIES #5

Andrew K. Roorda, M.D., Series Editor An Endoclip in Time Saves Nine

Swapna Gayam Matthew Weed Srinivasan Ganesan

INTRODUCTION CLIPS AVAILABLE FOR USE ndoclips are metallic accessory devices that are BY THE ENDOSCOPIST deployed via the working channel of the endo- Multiple endoclips, of varying shapes and sizes, are Escope. Once deployed, they exert pressure, bring- commercially available. Some endoclips have unique ing two mucosal surfaces together within the features. While most endoclips have two prongs, the gastrointestinal tract. In recent years the use of endo- TriClip (Cook Endoscopy, Winston-Salem, NC, USA) clips in endoscopy has increased. This is due to their has three prongs. The re-openable jaws of the Resolu- proven efficacy and safety profile in hemostatic appli- tion Clip (Boston Scientific, Natick, MA, USA) facili- cations along with multiple emerging non-hemostatic tate repositioning of the clip (if needed) and allow for indications. While in most instances they provide additional clip applications. The Olympus QuickClip definitive management by the endoscopist, they can (Olympus America, Center Valley, PA, USA) is rotat- also aid in subsequent radiographic (radiotherapy of able which improves maneuverability. malignancy or vascular embolization) and surgical (tumor resection) management. In some cases their use INDICATIONS FOR ENDOCLIP USE/PLACEMENT can spare the patient from a surgical procedure (in the case of perforations and anastomotic fistulas or leaks). Gastrointestinal Bleeding The purpose of this paper is to discuss endoclip fea- tures, indications, and complications. Upper Gastrointestinal Bleeding Acute non-variceal upper-GI bleeding (NVUGIB) Swapna Gayam, M.D., Matthew Weed, M.D., Srinivasan remains a significant cause of morbidity and mortality. Ganesan, M.D., Section of Digestive Diseases, Depart- It is responsible for approximately 300,000 hospital ment of Medicine, West Virginia University School of admissions and 30,000 deaths per year in the United Medicine, Morgantown, West Virginia. States.1 While predominantly caused by peptic ulcers

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(>80%), other sources of NVUGIB include angiodys- modalities. Additionally, several meta-analysis have plasias, Mallory-Weiss Syndrome (MWS), Dieulafoy been performed comparing endoclips to thermocoagu- lesions, mucosal inflammation and malignancy.2–3 lation and injection alone.7–8 The results of these Several endoscopic modalities can be utilized to analyses demonstrated endoclipping alone or in com- achieve hemostasis including injection of epinephrine, bination with injection was superior to injection alone thermal coagulation and mechanical devices such as in definitive hemostasis, rebleeding rates or need for band ligation and endoclips. surgery. There was no difference, though, comparing endoclips with thermotherapy alone or in combination. Peptic Ulcer Bleeding Thus, endoclips have proven to be a valuable modality Several studies have investigated the safety and effi- either alone or in combination for treating peptic ulcer cacy of endoclips in achieving hemostasis in peptic bleeding. ulcer bleeding. In 1988, Hachisu described the use of An additional use of endoclips in the setting of pep- an improved endoclip in 51 patients with gastrointesti- tic ulcers is the displacement of an adherent clot that nal bleeding.4 Permanent hemostasis was achieved obscures the source of bleeding (Figures 1A and 1B). It in 84.3% of patients with lesions that included: is therefore, readily accessible if the bleeding vessel is esophageal ulcer (1), Mallory-Weiss tear (4), gastric suddenly revealed eliminating the need to prepare and ulcer (24), duodenal ulcer (7), Dieulafoy lesion (3), exchange instruments through the channel. gastric cancer (3), and post-polypectomy sites (9). There have been some limitations to endoclip use In another study, Binmoeller et al. applied nearly in bleeding peptic ulcers, however. Ulcers in the pos- 255 endoclips in 88 patients with non-variceal upper terior duodenal bulb, posterior wall of the stomach and GI bleeding (78 for active spurting or oozing sources along the lesser curvature have had multiple reports of and 10 for non-bleeding visible vessel).5 Patients were failed deployment.7 followed for a mean duration of 397 days. Primary hemostasis was achieved in all patients. Only 5 Dieulafoy Lesions patients had recurrent bleeding of which 4 were suc- Dieulafoy lesions produce massive bleeding from a cessfully retreated with endoclips. During follow up it caliber-persistent arteriole that protrudes through nor- was determined that there was good clip retention. mal mucosa. They are typically found in the proximal There were no associated complications and clips did stomach along the lesser curvature.9 While only not impair mucosal healing of the ulcer. It was con- accounting for 1–2% of bleeding from an upper gas- cluded that endoclips were effective and safe method trointestinal source, their effects can be catastrophic of treating nonvariceal . and the need for diagnosis and effective therapy is cru- In 2000, Lai et al. evaluated the efficacy of rotat- cial. In 2000, Chung et al. compared the efficacy of able clips in bleeding peptic ulcers and demonstrated endoclips, banding and injection therapy in 24 patients that ultimate hemostasis was achieved in 87% and presenting with bleeding from Dieulafoy lesions.10 96% in spurting versus oozing vessels, respectively.6 Nine patients had endoclips placed, bands were used in Patients in shock on presentation had hemostasis rates, three and the remaining 12 cases received injection for the same subgroups (71% and 83%). Non-shock therapy. Initial hemostasis between mechanical versus patients had 100% hemostasis regardless of subgroup injection therapy was 91% and 75%, respectively. classification. Rebleeding rates after endoclip place- Recurrence in bleeding was 8.3% and 33.3%, respec- ment were low at 8%. No immediate complications, tively. While none of the patients in the mechanical tissue injury or impaired ulcer healing was noted dur- therapy group required surgical intervention, 17% of ing the study. the injection therapy group did. Park et al. studied While endoclips have proven safe and effective for endoclip therapy alone with epinephrine injections in the treatment of bleeding peptic ulcers, several ran- 32 patients presenting with bleeding from Dieulafoy domized controlled studies have been conducted to lesions.11 Primary hemostasis between endoclips and compare clip therapy to other endoscopic treatment injections was 93.8% and 87.5% respectively. Endo-

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Figure 1A. Large clot present in the stomach. Figure 1B. Movement of large clot using the Resolution Clip. clipping proved more effective in preventing recurrent of lower gastrointestinal bleeding. While surgical bleeding than injection, (0% v. 33 %, p < 0.05). Addi- resection has traditionally been indicated for recurrent tional studies have been performed comparing endo- bleeding, endoscopic hemostatic approaches appear to clips to other endoscopic modalities for controlling be a viable alternative. Multiple case reports have bleeding from Dieulafoy lesions. All have demon- described the effective use of endoclips to control strated efficacy in providing initial hemostasis and diverticular bleeding.16–18 Endoclip application can be reduction in rebleeding rates.7,12–13 Figure 2A shows to the culprit vessel within the dome16 or to close the an actively bleeding Dieulafoy lesion. Figure 2B margins of the diverticulum.18 While no head-to-head shows the same lesion with complete hemostasis after comparisons have been made with other endoscopic deployment of endoclips. therapeutic modalities, there is theoretical decreased risk of perforation. In addition, they can serve as a Mallory-Weiss Syndrome marker for either angiographic therapy or surgical 19 While bleeding from a Mallory-Weiss tear is usually approach if needed. self-limited, there are occasions when endoscopic ther- Post-polypectomy bleeding is another cause of apy is required due to active bleeding from a spurting clinically significant hematochezia. It can manifest or oozing blood vessel. Endoclips used to achieve immediately following removal of the polyp or occur hemostasis in this setting have been described. In one days to weeks later. Factors associated with higher bleeding risks include polyp location, number, size and study by Huang et al. in 2002, endoclipping and epi- 20 nephrine injections were compared.14 Another study in morphology (sessile or thick stalk). Early endo- 2008, by Cho et al., compared endoclips to band liga- scopic intervention can minimize blood loss from such tion.15 Both studies demonstrated equal efficacy in pri- bleeds. Endoclips have proven to be efficacious in pro- mary hemostasis and reduction in bleeding recurrence viding hemostasis to immediate and delayed post- between endoclips and their respective comparisons, polypectomy hemorrhage. Parra-Blanco et al. reported epinephrine injection or band ligation. 72 cases where endoclips were utilized in post- polypectomy bleeds.21 In cases involving peduncu- Lower Gastrointestinal Bleeding lated polyps, the clips were applied to the transected Diverticular bleeding is one of the most common types (continued on page 13)

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Figure 2A. Characteristic appearance of a Dieulafoy lesion Figure 2B. Complete hemostasis achieved following deploy- (active blood spurting from a tiny mucosal defect). ment of endoclips. stalk. In non-pedunculated sites endoclips were first leaks in seven patients.24 The median time to complete applied to any visible vessel, and then used to close the closure following clip placement, verified by radio- margins of the ulcerated site. In 2010, Chou et al. graphy, was 2.3 days. Two of the seven patients reported a case involving a large post-polypectomy required more than one session to achieve complete bleeding site that they were unable to primarily close closure of the leak. Figure 4A shows the site of anas- using a single endoclip.22 They described a novel tomotic leak after gastric pull-up surgery. Figure 4B approach whereby 4 clips were applied to the margin shows multiple endoclips deployed at the anastomotic of the ulcer site, followed by the deployment of a leak site. detachable Endoloop in a purse-string fashion around Endoclips have also been utilized to close chronic the clips to achieve hemostasis. fistulas. Hameed et al. detailed such a case of non- Endoclips, when applied prophylactically immedi- healing gastrocutaneous fistula from a gastrostomy ately after polypectomy, have also shown benefit in tube.25 They first used argon plasma coagulation to preventing post-polypectomy bleeding, even in antico- denude the fistulous tract, and then applied 4 endoclips agulated patients.23 Figure 3A shows a 1.5 centimeter to approximate the mucosal wall. This combination cecal polyp. Figure 3B shows the post-polypectomy resulted in successful permanent closure of the tract on site. Figure 3C shows the post polypectomy site after day two post-procedure. deployment of two endoclips. Perforations Post-Operative Complications Perforations in the gastrointestinal tract currently rep- When fistulas and anastomotic leaks occur, the main- resent an important indication for endoclip use. Most stay of closure is surgical. However, an initial attempt perforations are iatrogenic and are recognized compli- at closure with endoscopic clips may prove successful cations of diagnostic and therapeutic procedures [e.g., and save the patient from another extensive surgery. dilation of strictures and achalasia, endoscopic Rodella et al. first described the successful use mucosal resection (EMR) and endoscopic submucosal of endoclips to close esophagogastric anastomotic dissection (ESD), excision of tumors, polypectomy,

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Figure 3A. 1.5-cm sessile cecal polyp. Figure 3B. Post polypectomy site (following methylene blue/ normal saline injection, snare polypectomy, and cauteriza- tion with monopolar cautery). endoscopic sphinctorotomy, and endoscopic retro- grade cholangiopancreatography (ERCP) with stent placement, etc.]. Ideally, the defect should be closed as early as possible to minimize peritoneal contamination with digestive enzymes and fecal material.26–27 Surgical closure has traditionally been the stan- dard of treatment for perforations but immediate clo- sure of the defect with endoclips has been successfully reported. Binmoeller et al. described the first success- ful closure of an iatrogenic perforation using an endo- clip in 1993.28 In high risk patients, small localized perforations can be managed non-surgically with endoclipping.29 Defects as large as 10 cm have been successfully treated by endoclips.30 The endoclip is used by grasping the margins of the defect and approximating the tissue.31 Small perfora- Figure 3C. After prophylactic deployment of two endoclips to tions can be closed by placing clips across the center of oppose the polypectomy site. the gap whereas larger perforations require end to end placement of multiple clips.29 With closure of large defects, the endoscopist should start at one end of the ment of the edges is difficult or the perforation is larger defect and proceed across to the opposite end until the than the opened diameter of the endoclip.32 Elastic defect is closed. Endoclip deployment can sometimes bands, endoloops and fibrin glue can all be used along be difficult depending on the size and location (e.g., with endoclips to seal such difficult defects.33–36 posterior wall of the duodenal bulb) of the defect. A Figure 5A shows a colonic perforation site. Figure varix ligation cap device can be used to create suction 5B shows complete resolution of the colonic mucosal to facilitate endoclip deployment in cases where align- defect following endoclip application.

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Diagnostic Procedures Diagnostic EGDs rarely result in perforations but have been reported. Esophageal perforations secondary to diagnostic upper have been successfully closed with endoclips. When esophageal perforations are either too high or too low, they are not amenable to stent placement to cover the defect. Consequently, endoclips are the ideal choice in these situations.35 The risk of esophageal perforation with esophagogastro- duodenoscopy (EGD) alone is only 0.03% but increases to 17% with therapeutic interventions. 33–75% of the esophageal perforations are iatro- genic.37 There is almost no risk for duodenal perforation during a diagnostic EGD. However, this has been reported with diagnostic endoscopic ultrasound (EUS). Siebert and Sanders reported duodenal perforations Figure 4A. Site of anastamotic leak status post gastric occurring during diagnostic EUS that were successfully pull-up. treated with multiple endoclips and endoloops.38,39 For EUS guided fine needle aspiration biopsy, the risk of duodenal perforation is reported to be 0.44%.38 Von Renteln et al. described the use of over-the-scope clips to close duodenal perforations in a swine model.39 Perforation Due to Retroflexion Rectal and colonic perforations have been reported during colonoscopic retroflexion. These occur with a frequency of 0.1 per 1000 , even in the hands of experienced endoscopists.40 Prompt endo- clipping of these perforations has been reported. Tri- bonias et al. reported the use of endoclips to assist surgeons in performing full thickness suturing intraop- eratively.41 Ahlawat et al. described a case of rectal perforation during routine screening which was immediately closed with multiple endo- Figure 4B. Following endoclip deployment at site of anasto- clips.42 Several other cases of iatrogenic rectal perfo- motic leak. rations that were treated with endoclips (with or without endoloops) have been described recently.43–45 toms of sepsis are present. Using endoclips to close these perforations has been successfully reported even Colon Perforations when they are >10 mm and in all segments of the colon Colonic perforations during diagnostic and therapeutic and rectum.46 Yoshikane reported the first successful colonoscopies (EMR 58%, ESD 21%, polypectomy case of colonic perforation repair with clips followed 18%, hot biopsy 1.5%, argon plasma coagulation by Mana et al. and several others.47–49 Raju et al. used 1.5%) were reported to be between 0.01% and 3%.46 a porcine model to demonstrate the use of endoclips to Surgical treatment is recommended if signs and symp- close colon perforations.50 Endoclips may fall off

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Figure 5A. Colonic perforation site. Figure 5B. Complete resolution of colonic mucosal defect following endoclip deployment. spontaneously and get eliminated in 4 weeks to 4 been published about EMR induced perforations months.49 treated with endoclips.56–60 In a large case series of 7859 colonoscopies in Endoclips can also be used to close large defects 2007, Madgeburg et al. reported that most colonic per- secondary to EMR to prevent bleeding or perforation. forations occurred during therapeutic colonoscopies, Fuju et al. described a unique technique using a spe- especially with EMR, but in most cases were amenable cially designed 8-ring to connect two endoclips to to endoclipping.51 close the defect.61 Another technique using endoloops and endoclips was proposed by Hurlstone et al. in EMR and ESD 2002.62 EMR is a popular therapeutic technique used for high EMR can also be performed through a retroflexed grade dysplasia and early stage cancer within the gas- colonoscope. Coumaros and Tsesmeli described a case of such a procedure resulting in perforation which was trointestinal tract. It is an alternative to surgery for the 63 removal of superficial gastrointestinal neoplasms.52 immediately closed with endoclips. ESD allows en- Reported perforation rates for EMR are 0.3–0.5% and bloc resection of lesions >2 cm which makes it more for ESD, 4–10%. Small perforations recognized dur- desirable than EMR for large lesions. However, it is also associated with a higher rate and size of perfora- ing the procedure can be successfully sealed with 54,64 endoscopic clips.53 tions. Nonetheless, a good number of these perfo- Shimizu et al. reported three perforations in 185 rations can be managed endoscopically. Minami et al. patients who underwent EMR between 1994 and reported the first case series of gastric perforations 54 post ESD managed endoscopically with clips with a 2003. All 3 defects were closed using the clipping 56 technique. In 2003, Tsunada et al. reported 7 cases of 98.3% success rate. The immediate endoscopic man- gastric perforation secondary to EMR for early gastric agement of such iatrogenic perforations is a key factor in the success of endoscopic resection of early gastric cancer, one of the first reported case series using endo- 64 clips for EMR induced perforations.55 The largest per- cancer by ESD. According to Chung et al., perfora- foration was 25 mm and the maximum number of clips tion related to ESD can no longer be regarded as an used was 11. Several other case reports and series have (continued on page 21)

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obstacle to performing ESD, because this can be com- Dilation pletely managed by endoscopic clipping in most cases, Endoscopic dilation, as necessitated by benign and 65 with favorable outcomes. Several other reports of malignant etiologies, also raises the risk of perforation. ESD related perforations have been reported to be Mucosal perforation is a major complication of endo- 66–71 treated by endoclipping. scopic balloon dilation in the .79 Fischer et ERCP al. reported a case of esophageal perforation due to esophageal dilation in a patient with achalasia which ERCP-related duodenal perforation is a well-recog- was immediately closed with endoclips.35 nized albeit rare complication. Lateral and medial wall Strictures form occasionally at the gastrojejunos- perforations can occur due to the introduction of the tomy stomal site after Roux-en-Y gastric bypass. Iatro- duodenoscope (0.1%), endoscopic sphincterotomy genic perforation during dilation of such strictures 26,72 (<1%) or guidewire trauma. These perforations are ranges from 3–12%. Tang et al. reported a case of gas- severe and usually require immediate surgical repair. trojejunal anastomosis perforation during dilation and However, endoscopic closure with endoclips (with or immediate closure with endoclips.80 Cipolletta et al. without endoloops) can be attempted during the proce- described two patients with esophagojejunal anasto- dure. The endoclip is designed to be used through the motic strictures post Roux-en-Y esophagojejunostomy forward-viewing endoscope. Consequently, endoclip which were treated conservatively with metal endo- deployment is more difficult when a side-viewing clips in a single session.79 Qadeer et al. compiled a endoscope is used and therefore requires a higher level pooled analysis of several reports of esophageal perfo- 27,34,73 of skill and expertise by the endoscopist. rations caused spontaneously and iatrogenically 81 Stent Perforations (including dilation), all treated with clips. Duodenal perforation caused by biliary stents is very NOTES rare (1%) and is usually secondary to migration of the stent, leading to impaction and puncturing of the In Natural Orifice Transluminal Endoscopic Surgery duodenal wall. This can happen with both plastic and (NOTES), safe closure of gastrostomy is essential if metal stents and can occur after either endoscopic or the transgastric route is used. Experimental NOTES percutaneous placement.32,72 Migration of the stent to done on pig models in multiple studies showed that the ileum and colon causing perforation has also been endoscopic clips provide a superior histopathological 82 reported.74–76 Most stent related perforations are outcome. In 2009, an over-the-scope clip was used retroperitoneal. for gastric closure in NOTES and was shown to be easy, reliable and comparable to surgical sutures.83–84 Polypectomy Perforations can also occur during endoscopic Non-iatrogenic Perforations polypectomy. The Munich Polypectomy Study Treated by Endoclipping (MUPS) in 2005 reported a 1.1% perforation rate for Non-iatrogenic spontaneous perforations have also 3976 snare polpectomies, 5 of which were treated with been successfully treated with clips. endoscopic clipping.77 Katsinelos et al. reported a case Addley et al. reported a case of anterior gastric of gastric polypectomy induced perforation in the gas- perforation sustained during a stab injury to the ante- tric antrum that was treated with endoclipping.78 rior wall that was treated with endoclips.85 Fish bone Chuan-San Fan et al. described a case of perforation impaction is a common cause of GI perforation in the on the posterior wall of the duodenal bulb after snare Far East. Sung and Shimamoto reported two cases of resection of a 2.5-cm polyp. In this particular case, a fish bone induced esophageal perforations that were band ligator device and elastic band was used to close closed with endoclips.86–87 Successful closure of a the gap due to limited space and tangential angle of the spontaneous esophageal perforation caused by Boer- location.33 haave’s syndrome has also been reported.88

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Other Endoclip Applications common complications, stent migration. This is espe- cially true in the case of covered stents, which were Preoperative Endoclipping designed to overcome tumor in-growth associated with (Including Localization of Malignancy) uncovered stents. Stent migration can lead to increased Preoperative endoclip deployment can assist surgeons morbidity (obstructive symptoms or perforation). It in performing full thickness suturing intraopera- also may result in repeat endoscopic examinations tively.41 Matsui and Kikuchi et al. reported the use of which can inflate healthcare costs and lead to a endoclips to delineate the line of resection in laparo- decreased quality of life, especially in the palliative scopic gastrectomy.89–90 A novel magnetic marking care setting. clip-detection system was proposed by Ohdaira Kim et al. prospectively evaluated the clinical effi- and Nagai for tumor detection during surgery.91–92 cacy of endoscopic clipping for the prevention of cov- Tabibian et al. advocate the placement of an endoclip ered stent migration in the treatment of malignant 96 into the mucosa around small colonic malignancies gastric outlet obstruction (GOO). The site of obstruc- prior to surgery as this aids the surgeon in localizing tion was at the pylorus and antrum (n = 18), duodenal them when they might otherwise be difficult to find by bulb (n = 1), and in the second portion of the duode- palpation.93 num (n = 6). Immediately following stent deployment, endoclips were applied at the proximal end of the Radiographic Localization of Colonic Tumors enteral stent to fix the gastrointestinal mucosa. The When an obstructing tumor proximal to the recto-sig- stent was a double-layered combination stent (com- moid colon prevents completion of the endoscopic prising an outer uncovered and an inner covered stent). exam, accurate localization becomes challenging. This Three clips were used for each stent and the endo- has important surgical management implications in scopist clipped the wire mesh of the stent and the nor- that the anatomical location of the lesion is not well- mal mucosa together at three different points. defined. Knopp et al. described placement of an endo- Technical success (defined as satisfactory deployment clip on the first haustral fold (just distal to the lesion) and precise positioning at the location of the stenosis) for radiographic purposes. Subsequent flat plate of the and clinical success (defined as the ability to tolerate abdomen revealed the endoclip in the area of the distal oral intake without vomiting) were 100% and 88%, transverse colon in close proximity to the splenic flex- respectively. Subsequent stent migration did not occur ure. This approach appears to be useful when endo- in any of the patients. Anchoring the stent to normal scopic localization of a colorectal lesion is unclear. tissue with endoclips allows enough time for tissue or tumor to grow into mesh struts and provide adequate Endoclip-assisted Biliary Cannulation anchorage for the self-expanding metal stents (SEMS). The presence of an intradiverticular papilla (IDP) during It also avoided the patient inconvenience of having a ERCP can present a challenge to the endoscopist with catheter or silk thread protruding from the nasal cavity, respect to cannulation of the common bile duct. Scotin- thus improving patient tolerance. iotis and Ginsberg reported the first case of endoclip- Park et al. also reported no early stent migration in assisted biliary cannulation.94 This technique uses one their clipping group (0/19 patients) in contrast to their or more endoclips to facilitate a temporary and favor- non-clipping group (5/19 patients).97 This study was able change in the anatomical position of the major notable in that it included nine cases of malignant papilla, thus enabling successful cannulation. Huang et colonic obstruction. al. recently described two additional cases that con- Kato et al. reported on the utility of endoclips in firmed the utility of this technique in cases of IDP.95 preventing esophageal stent migration.98 Nine patients underwent SEMS implantation. After deployment of Prevention of Luminal Stent Migration the SEMS, endoscopic clips were used to fix the upper With the increasing use of endoluminal stents, we are end of the stent to the esophageal mucosa. No stent also more frequently encountering one of its most migration was observed in any of the patients.

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Sebastian and Buckley applied endoclips at the Frizzell and Darwin describe a technique where a Res- cranial and caudal ends of SEMS in three patients with olution Clip was used to ensure proper placement of rectal cancer.99 Subsequent stent migration did not nasojejunal feeding tube and jejunal extension through occur in any of these patients. a percutaneous endoscopic gastrostomy (PEG-J).105 This technique takes advantage of the ability of the Fluoroscopic Markers in Luminal Resolution Clip to be open and closed, like biopsy for- Stent Deployment ceps, without inadvertent deployment. After the jeju- Given their metallic composition, endoclips have also nal feeding tube is passed into the gastric body, a demonstrated utility as fluoroscopic markers prior to Resolution Clip is passed through a pediatric colono- stent deployment.100 scope and is used to grasp a suture attached to the feed- ing tube. After the clip is closed on the suture, the clip Ambulatory Colonic Manometry is withdrawn back into the endoscope. The endoscope While ambulatory colonic manometry can provide is then passed to the ligament of Treitz, where the clip useful pathophysiologic information regarding colonic is advanced, opened, and deployed on the jejunal motor function, probe displacement during prolonged mucosa. The authors noted good long-term results, recording can prove problematic. Such displacement with no migration up to 46 days after tube placement. likely occurs because of propulsive forces which cause Ginsberg et al. describe a similar technique of endoclip the catheter to move distally. Rao et al. compared two assisted placement of enteral feeding tubes.106 Figure study groups [one group whose probes were anchored 6 shows a jejunostomy tube anchored to the jejunal to the colonic mucosa using endoclips (n = 14) and mucosa via a Resolution Clip. another group whose probes were left unattached in the colon (n = 16)].101 The magnitude of transducer Incomplete Colonoscopic Examinations displacement was subsequently assessed by fluoro- When anatomic landmarks such as the ileocecal valve scopic localization and a displacement score was cal- or appendiceal orifice are not visualized during culated. In patients without clipping, the mean colonoscopy, the endoscopist cannot say with confi- displacement score was 1.6, implying displacement of dence that the entire colon has been examined. Tabbian transducers by 1.6 colonic segments relative to their et al. described the use of endoclips in such cases.93 initial location. In contrast, there was no displacement of transducers in those who received endoclipping. The authors concluded that endoscopic mucosal clip- ping was safe and effective for prevention of probe displacement and ensures more accurate temporospa- tial resolution of data for prolonged colonic manome- try recording. Other authors have reported similar efficacy of colonic manometric endoclipping.102–103 24-hour Ambulatory Esophageal pH Monitoring Endoclips have also been utilized in 24-hour ambula- tory esophageal pH monitoring to anchor the electrode to the mucosa.104 Placement of Jejunal Feeding Tubes Endoscopic placement of jejunal feeding tubes can be challenging given the high rate of proximal migration Figure 6. Anchoring of jejunostomy tube to jejunal mucosa which can occur even during endoscope withdrawal. using an endoclip.

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Following the procedure, the location of the endoclip quent angiography.110 This has potential therapeutic was established radiographically. This facilitates cor- implications with respect to guiding embolization. relation of endoscopic and radiographic impression and helps determine whether further evaluation is Modification of Obstructive needed (e.g. repeat colonoscopy or barium enema). Post-surgical Anatomy Zanati et al. describe a case where post-surgical anatomy Delineation of Gastrointestinal was successfully modified by the deployment of endo- Malignancies Prior to Radiotherapy clips.111 The patient they describe developed gastric out- Endoclips can also be used to delineate gastrointestinal let obstruction shortly after Billroth II gastrojejunostomy malignancies prior to radiotherapy. Weyman and Rao for gastric adenocarcinoma. On upper endoscopy, a describe a case where the esophageal tumor margins redundant jejunal fold was noted to be obstructing were readily identified on upper endoscopy after bar- the inlet to the efferent limb. Given poor nutritional sta- ium esophagram failed to localize the full extent of the tus, the risk of re-operation was substantial and a deci- tumor.107 One endoclip was placed at the proximal sion was made to attempt endoscopic revision of the margin and another at the distal margin of the tumor. anastomosis using endoclips. Multiple endoclips were deployed with resultant fixation of redundant jejunal Clip-assisted Zenker’s Diverticulotomy folds to open lumen of the efferent limb. While the Tang and Lara describe a case of a patient with a symp- patient died six months after surgery from metastatic dis- tomatic residual Zenker’s diverticulum (ZD) who ease, he was able to tolerate a full diet without recurrence underwent flexible endoscopic clip-assisted divertic- of vomiting following endoclip placement. ulectomy (ECD).108 This resulted in complete septum dissection with resolution of all esophageal symptoms and no complications. The authors also propose the COMPLICATIONS OF ENDOCLIP PLACEMENT use of ECD for small ZD (less than 2 cm), for patients Endoclip placement has proven to be safe in a variety with a larger ZD who prefer stepwise dissection, and of clinical settings and potential complications are for ECD of lower parts or bottom of the septum (bot- minimal. Since endoclips only adhere to the mucosa tom ECD). and submucosa, the risk of perforation is low. One should use caution when utilizing cautery in close Foreign Body Management proximity to endoclips. This is especially important in Ingestion of sharp foreign bodies can pose a manage- hemostasis when electrocautery may be used in com- ment challenge to the endoscopist. At times multiple bination with endoclips. attempts at retrieving the foreign bodies using multiple Gill et al. looked at the compatibility of endoclips retrieval modalities (snares, nets, baskets, and forceps) in magnetic resonance imaging.112 They studied the will fail. Thornton et al. describe a case where a physical deflection and strength of attraction of Resolution Clip was used to grasp a razor blade frag- various endoclips [Resolution Clip, TriClip, ment.109 The clip was opened and repositioned several QuickClip, and Ethicon Endo-Surgery Clip (Ethicon times until the hole in the razor blade was clasped and Endo-Surgery, Cincinnati, OH, USA)] in an MRI secured. The clip was placed in the closed and locked using a pig model. They found that the Ethicon position but not deployed. Once the razor blade was Endo-Surgery clip was compatible with MRI. They brought back into the esophagus, the endoscope, over- also showed that all other clips showed deflection in a tube, clip, and blade were all removed as a system. magnetic field. The TriClip demonstrated detachment from gastric tissue, and it was thus felt by the authors Localization of Suspicious to be considered MRI incompatible. This is an impor- Vascular Lesions Prior to Embolization tant consideration, especially in light of the fact that in Endoclips placed at the site of a suspicious vascular lesion have proven useful for localization on subse- (continued on page 26)

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some instances endoclips can remain attached to the Table 1. Indications for Endoclip Use/Placement. mucosa for protracted periods of time (up to 26 months has been reported).31 • Gastrointestinal bleeding – Movement of clot to reveal bleeding source (in position for rapid endoclipping if active CONCLUSION re-bleeding occurs) Endoclips have proven to be one of the most valuable – Non-variceal upper gastrointestinal bleeding accessories available to the endoscopist. Their utility • Peptic ulcer disease has transcended initial hemostatic indications, evolv- • Dieulafoy lesions ing over time to encompass numerous other luminal • Mallory-Weiss tear and biliary applications (Table 1). These applications, – Lower gastrointestinal bleeding while at times prove definitive, often guide further • Diverticular bleeding management by our radiological and surgical col- • Post-polypectomy bleeding leagues. We must strive to refine existing clipping • Post-operative complications techniques and continue to develop new and beneficial – Anastomotic leaks endoclip indications. – Fistulas

• Perforations Acknowledgment – Diagnostic endoscopy The authors would like to acknowledge Max Miranda, – Therapeutic endoscopy M.D. for his valuable input in the preparation of this • Dilation manuscript. • EMR/ESD • Polypectomy – Secondary to stent migration References – NOTES 1. DiMaio CJ, Stevens PD. Nonvariceal upper gastrointestinal – Trauma bleeding. Gastrointest Endosc Clin N Am 2007;17:253-72, v. 2. Yuan Y, Wang C, Hunt RH. Endoscopic clipping for acute non- – Fish bone impaction variceal upper-GI bleeding: a meta-analysis and critical appraisal – Boerhaave’s syndrome of randomized controlled trials. Gastrointest Endosc 2008; 68:339-51. • Other endoclip applications 3. Esrailian E, Gralnek IM. Nonvariceal upper gastrointestinal – Preoperative endoclipping (including localization bleeding: epidemiology and diagnosis. Gastroenterol Clin North Am 2005;34:589-605. of malignancy) 4. Hachisu T. Evaluation of endoscopic hemostasis using an – Radiographic localization of colonic tumors improved clipping apparatus. Surg Endosc 1988;2:13-7. – Endoclip-assisted biliary cannulation 5. Binmoeller KF, Thonke F, Soehendra N. Endoscopic hemoclip treatment for gastrointestinal bleeding. Endoscopy 1993;25:167- – Prevention of luminal stent migration 70. – Fluoroscopic markers in luminal stent deployment 6. Lai YC, Yang SS, Wu CH, Chen TK. Endoscopic hemoclip treat- – Ambulatory colonic manometry ment for bleeding peptic ulcer. World J Gastroenterol 2000;6:53- 6. – 24-hour ambulatory esophageal pH monitoring 7. Sung JJ, Tsoi KK, Lai LH, Wu JC, Lau JY. Endoscopic clipping – Placement of jejunal feeding tubes versus injection and thermo-coagulation in the treatment of non- – Incomplete colonoscopic examinations variceal upper gastrointestinal bleeding: a meta-analysis. Gut 2007;56:1364-73. – Delineation of gastrointestinal malignancies prior 8. Barkun AN, Martel M, Toubouti Y, Rahme E, Bardou M. Endo- to radiotherapy scopic hemostasis in peptic ulcer bleeding for patients with high- – Clip-assisted Zenker’s diverticulotomy risk lesions: a series of meta-analyses. Gastrointest Endosc 2009;69:786-99. – Foreign body management 9. Lara LF, Sreenarasimhaiah J, Tang SJ, Afonso BB, Rockey DC. – Localization of suspicious vascular lesions prior Dieulafoy lesions of the GI tract: localization and therapeutic out- to embolization comes. Dig Dis Sci 2010;55:3436-41. 10. Chung IK, Kim EJ, Lee MS, et al. Bleeding Dieulafoy’s lesions – Modification of obstructive post-surgical anatomy and the choice of endoscopic method: comparing the hemostatic efficacy of mechanical and injection methods. Gastrointest Endosc 2000;52:721-4.

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24. Rodella L, Laterza E, De Manzoni G, et al. Endoscopic clipping Practical Points of anastomotic leakages in esophagogastric surgery. Endoscopy 1998;30:453-6. • Multiple hemostatic and non-hemostatic indications 25. Hameed H, Kalim S, Khan YI. Closure of a nonhealing gastrocu- tanous fistula using argon plasma coagulation and endoscopic exist for endoclip use, a few of which do not require hemoclips. Can J Gastroenterol 2009;23:217-9. clip deployment. 26. Lee TH, Bang BW, Jeong JI, et al. Primary endoscopic approxi- mation suture under cap-assisted endoscopy of an ERCP-induced • Endoclip deployment has proven utility in both the pro- duodenal perforation. World J Gastroenterol 2010;16:2305-10. phylaxis and treatment of gastrointestinal bleeding. 27. Katsinelos P, Paroutoglou G, Papaziogas B, Beltsis A, Dimiropoulos S, Atmatzidis K. Treatment of a duodenal perfora- • While emergent surgery has traditionally been the tion secondary to an endoscopic sphincterotomy with clips. World J Gastroenterol 2005;11:6232-4. standard of care for iatrogenic endoscopic perfora- 28. Binmoeller KF, Grimm H, Soehendra N. Endoscopic closure of a tions, immediate endoclip closure is currently the treat- perforation using metallic clips after snare excision of a gastric ment of choice in most patients. leiomyoma. Gastrointest Endosc 1993;39:172-4. 29. Raju GS, Gajula L. Endoclips for GI endoscopy. Gastrointest • Endoclips serve as excellent markers in many clinical Endosc 2004;59:267-79. 30. Areia M, Amaro P, Figueiredo P, et al. [Spontaneous extensive scenarios and guide subsequent radiographic or surgi- esophageal tear with upper digestive haemorrhage treated by cal management. endoclip application]. Rev Esp Enferm Dig 2007;99:233-4. 31. Devereaux CE, Binmoeller KF. Endoclip: closing the surgical • Endoclips have a favorable safety profile and are asso- gap. Gastrointest Endosc 1999;50:440-2. ciated with minimal complications. 32. Roses LL, Ramirez AG, Seco AL, et al. 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45. Katsinelos P, Chatzimavroudis G, Zavos C, Paroutoglou G, plasms: Korean ESD Study Group multicenter study. Gastroin- Kountouras J. Closure of an iatrogenic rectal perforation by using test Endosc 2009;69:1228-35. the endoloop/clips technique. Gastrointestinal Endoscopy 2009; 66. Saito Y, Uraoka T, Yamaguchi Y, et al. A prospective, multicen- 70:405-6. ter study of 1111 colorectal endoscopic submucosal dissections 46. Trecca A, Gaj F, Gagliardi G. Our experience with endoscopic (with video). Gastrointest Endosc 2010;72:1217-25. repair of large colonoscopic perforations and review of the liter- 67. Fujishiro M, Yahagi N, Nakamura M, et al. Endoscopic submu- ature. Techniques in Coloproctology 2008;12:315-21. cosal dissection for rectal epithelial neoplasia. Endoscopy 47. Yoshikane H, Hidano H, Sakakibara A, et al. Endoscopic repair 2006;38:493-7. by clipping of iatrogenic colonic perforation. Gastrointestinal 68. Fujishiro M, Yahagi N, Kakushima N, et al. 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Gastrointest Endosc 1999;50:410-3. scopic clips for closing esophageal perforations: case report and 61. Fujii T, Ono A, Fu KI. A novel endoscopic suturing technique pooled analysis. Gastrointestinal Endoscopy 2007;66:605-11. using a specially designed so-called “8-ring” in combination with 82. Dray X, Krishnamurty DM, Donatelli G, et al. Gastric wall heal- resolution clips (with videos). Gastrointest Endosc 2007; ing after NOTES procedures: closure with endoscopic clips pro- 66:1215-20. vides superior histological outcome compared with threaded tags 62. Hurlstone DP, Lobo AJ. A new technique for endoscopic resec- closure. Gastrointest Endosc 2010;72:343-50. tion of large lateral spreading tumors of the colon: duel intubation 83. von Renteln D, Schmidt A, Vassiliou MC, Gieselmann M, Caca colonoscopy with endoclip-assisted “loop suturing” method. Am K. 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85. Addley J, Ali S, Lee J, Taylor M, Lowry P, Mitchell RM. Endo- 106. Ginsberg GG, Lipman TO, Fleischer DE. Endoscopic clip- scopic clip closure of penetrating stab wound to stomach. assisted placement of enteral feeding tubes. Gastrointest Endosc Endoscopy 2008;40 Suppl 2:E219-20. 1994;40:220-2. 86. Sung HY, Kim JI, Cheung DY, et al. Successful endoscopic 107. Weyman RL, Rao SS. A novel clinical application for endoscopic hemoclipping of an esophageal perforation. Dis Esophagus mucosal clipping. Gastrointest Endosc 1999;49:522-4. 2007;20:449-52. 108. Tang SJ, Lara LF. Flexible endoscopic clip-assisted Zenker’s 87. Shimamoto C, Hirata I, Umegaki E, Katsu K. Closure of an diverticulotomy (with videos). Gastrointest Endosc 2008;67: esophageal perforation due to fish bone ingestion by endoscopic 704-8. clip application. Gastrointest Endosc 2000;51:736-9. 109. Thornton JG, Kale H, Ferguson DR. Ingested foreign bodies: a 88. Sriram PV, Rao GV, Reddy ND. Successful closure of sponta- new use of endoscopic clips for retrieval. Endoscopy 2007;39 neous esophageal perforation (Boerhaave’s syndrome) by endo- Suppl 1:E164-5. scopic clipping. Indian J Gastroenterol 2006;25:39-41. 110. Golder S, Strotzer M, Grune S, Zulke C, Scholmerich J, Mess- 89. Matsui H, Okamoto Y, Nabeshima K, Kondoh Y, Ogoshi K, mann H. Combination of colonoscopy and clip application with Makuuchi H. Endoscopy-assisted gastric resection: a safe and angiography to mark vascular malformation in the small intestine. reliable procedure for tumor clearance during laparoscopic high Endoscopy 2003;35:378. distal or proximal gastrectomy. Surg Endosc 2009;23:1146-9. 111. Zanati SA, Ganc RL, Kortan P. Endoscopic modification of a 90. Kikuchi S, Hirai K, Kuroyama S, et al. Role of endoscopic clip- Billroth II gastrojejunostomy by using metallic clips. 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Endoscopic clip-assisted biliary can- nulation: externalization and fixation of the major papilla from within a duodenal diverticulum using the endoscopic clip fixing device. Gastrointest Endosc 1999;50:431-6. 95. Huang CH, Tsou YK, Lin CH, Tang JH. Endoscopic retrograde cholangiopancreatography (ERCP) for intradiverticular papilla: endoclip-assisted biliary cannulation. Endoscopy 2010;42 Suppl 2:E223-4. 96. Kim ID, Kang DH, Choi CW, et al. Prevention of covered enteral stent migration in patients with malignant gastric outlet obstruc- tion: a pilot study of anchoring with endoscopic clips. Scand J Gastroenterol 2010;45:100-5. 97. Park SY, Park CH, Cho SB, et al. [The usefulness of clip appli- cation in preventing migration of self-expandable metal stent in CALL FOR PAPERS patients with malignant gastrointestinal obstruction]. Korean J Gastroenterol 2007;49:4-9. ANNOUNCING AN EXCITING 98. Kato H, Fukuchi M, Miyazaki T, et al. Endoscopic clips prevent self-expandable metallic stent migration. Hepatogastroenterol- NEW DIRECTION FOR ogy 2007;54:1388-90. PRACTICAL GASTROENTEROLOGY 99. Sebastian S, Buckley M. Endoscopic clipping: a useful tool to prevent migration of rectal stents. Endoscopy 2004;36:468. We are launching a new series on original 100. Raijman I, Baptista A, Bonilla Y, et al. Non-hemostatic use of endoclips. Gastrointestinal Endoscopy 2005;61:Ab236-Ab. digestive diseases research. Research can be 101. Rao SS, Singh S, Sadeghi P. Is endoscopic mucosal clipping use- prospective or retrospective as well as clinical in ful for preventing colonic manometry probe displacement? J Clin nature. Outcomes or population based research is Gastroenterol 2010;44:620-4. also welcome. Please provide a cover letter that 102. De Schryver AM, Samsom M, Akkermans LM, Smout AJ. Endo- clips in prolonged colonic manometry. Gastrointest Endosc briefly summarizes the important aspects of the 2000;52:819-20. manuscript with recommendations for up to three 103. Fajardo N, Hussain K, Korsten MA. Prolonged ambulatory reviewers who are qualified in the field as well colonic manometric studies using endoclips. Gastrointest Endosc as three reviewers who may have a conflict of 2000;51:199-201. 104. McLauchlan G, Buchanan NM, Crean GP, McColl KE. An endo- interest with your study. Please send manuscripts scopic procedure for accurate localisation of intraluminal pH electronically to Dr. Uma Sundaram, attention electrodes. Endoscopy 1987;19:124-6. Cristin Murphy (telephone: 304.293.4123) to the 105. Frizzell E, Darwin P. Endoscopic placement of jejunal feeding following e-mail address: [email protected] tubes by using the Resolution clip: report of 2 cases. Gastrointest Endosc 2006;64:454-6.

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