A novel double-endoloop technique for natural orifice transluminal endoscopic surgery gastric access site closure

ORIGINAL ARTICLE: Experimental Endoscopy

A novel double-endoloop technique for natural orifice transluminal endoscopic surgery gastric access site closure Tomas Hucl, MD, PhD, Marek Benes, MD, Matej Kocik, MD, Martin Krak, MD, Jana Maluskova, MD, Eva Kieslichova, MD, Martin Oliverius, MD, Julius Spicak, MD, PhD Prague, Czech Republic

Background: Effective and safe access site closure is critical for clinical application of natural orifice transluminal endoscopic surgery. Objective: The current study evaluated a simple novel technique of gastrotomy closure. Design: Feasibility study with a survival animal model. Setting: Animal laboratory. Subjects: Ten female domestic pigs. Interventions: Endoscopic closure of a gastrotomy incision was evaluated in 10 pigs in a survival study. A standard double-channel endoscope was advanced into the peritoneal cavity through an incision made by a needle-knife and an 18-mm dilation balloon. After peritoneoscopy and salpingectomy, gastric closure was performed by using an endoscopic grasper and sequential application of 2 endoloops. After a follow-up period of 1 to 3 weeks, the pigs were killed for postmortem examination. Main Outcome Measurements: Feasibility, efficiency, and safety of a novel closure technique. Results: Correct positioning and delivery of endoloops was achieved in all animals in a median time of 17 minutes (range 13-25 minutes). All animals survived without complications. Postmortem examination demonstrated patent full-thickness gastric closure without any evidence of infection. Limitations: Feasibility study with a small number of subjects in a porcine model. Conclusion: Double endoloop technique represents a novel, simple, safe, and efficient means of gastric access site closure in natural orifice transluminal endoscopic surgery. (Gastrointest Endosc 2010;71:806-11.)

Traditional open surgery has been challenged by minimally invasive surgery for its proven advantages. Laparo-

Abbreviations: NOTES, natural orifice transluminal endoscopic surgery. DISCLOSURE: J. Spicak was supported in part by grant NS 10525-3 from the Czech Ministry of Health. All authors disclosed no financial relationships relevant to this publication. Copyright © 2010 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 doi:10.1016/j.gie.2009.10.058 Received August 28, 2009. Accepted October 27, 2009. Current affiliations: Departments of Hepatology and Gastroenterology (T.H., M.B., J.S.), Transplantation Surgery (M.K., M.O.), Anesthesiology (M.K., E.K.), and Pathology (J.M.), Institute for Clinical and Experimental Medicine, Prague, Czech Republic. Reprint requests: Tomas Hucl, MD, PhD, Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, Videnska 9, 140 21, Prague 4, Czech Republic.

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scopic surgery is generally less traumatic than open surgery and therefore is associated with fewer local and systemic complications, less postoperative pain, better recovery, and better cosmesis.1 Several abdominal and pelvic procedures are now routinely performed laparoscopically.2 In recent years, a novel minimally invasive technique has been developed that may be even less invasive than traditional laparoscopic surgery. This technique takes advantage of natural orifices and is referred to in the literature as natural orifice transluminal endoscopic surgery (NOTES).3 A variety of surgical procedures that use natural orifices has been performed to date in animals and humans.4 Because NOTES often gains access to the abdominal cavity through the stomach, closure of the transluminal access site has been a major concern.4 Efficacy and safety are crucial before NOTES can gain wide acceptance as a therapeutic alternative. Various closure techniques of gaswww.giejournal.org

Hucl et al

tric and colonic incisions based on suturing, stapling, clipping, plugging, stenting, or tunneling have been evaluated with various closure times, technical difficulty, efficacy, and expense.5,6 Because of the uncertain efficacy and safety of gastric and colonic closure, vaginal access with hand-sutured closure has been preferred in most human NOTES procedures.7,8 The aim of our study was to evaluate the feasibility, efficiency, and safety of a novel simple closure technique using endoscopic accessories that are widely available.

MATERIAL AND METHODS

Novel double-endoloop technique for NOTES gastric access site closure

Capsule Summary What is already known on this topic ●

Effective and safe closure of transluminal access sites is necessary before natural orifice transluminal endoscopic surgery (NOTES) can gain acceptance.

What this study adds to our knowledge ●

In 10 pigs, endoscopic closure of a gastrotomy incision using a grasper and sequential application of 2 endoloops resulted in patent full-thickness closure without evidence of infection.

Animals and preparation The study was performed in female pigs weighing between 23 and 40 kg. The animals were fed a liquid diet and then fasted overnight before the procedure. Before endoscopy, ketamine (10 mg/kg) and azaperone (4 mg/kg) were injected intramuscularly. The animals were endotracheally intubated and were administered general anesthesia with isoflurane (0.8%–1.5%) and fentanyl (3–5 mL/h). Antibiotics (1 g cefazolin) were administered intravenously 30 minutes before the procedure.

Procedure All procedures were performed in aseptic conditions with a standard double-channel endoscope (CF 2T160I; Olympus Optical Co, Tokyo, Japan). The stomach was irrigated with 1 L of disinfectant solution (10% Betadine; Egis Pharmaceuticals, Budapest, Hungary) and the percutaneous endoscopic gastrostomy (PEG) technique was used to obtain access to the peritoneal cavity.9 Briefly, after transillumination, the anterior wall of the stomach was punctured with a needle under endoscopic vision and a guidewire (Jagwire; Boston Scientific, Natick, Mass) was introduced through the needle into the stomach. The guidewire was secured with a snare, pulled through the endoscope working channel, and left in place to guide the subsequent incision. A Veress needle was introduced percutaneously into the peritoneal cavity in the umbilical region by using standard techniques. Pneumoperitoneum was established and continuously maintained by using a carbon dioxide insufflator containing a built-in manometer (UHI-3; Olympus). A gastric wall incision was made alongside the guidewire with a triple-lumen needle-knife (Microknife XL; Boston Scientific) followed by balloon dilation with an 18-mm CRE balloon (Boston Scientific). The endoscope was advanced into the peritoneal cavity, which was briefly explored, and the fallopian tubes on both sides were identified. An endoloop (HX-400U-30; Olympus) was placed on one of the fallopian tubes and tightened. A salpingectomy was completed by using a snare. Gastric wall closure was performed by two sequentially delivered endoloops (Olympus). First, an endoscopic www.giejournal.org

grasper was advanced through an open endoloop. One edge of the incision was grasped and pulled through the endoloop toward the endoscope. The endoloop was closed and then released (Fig. 2). This maneuver resulted in control of one of the edges in a ligature. Next, the other edge of the incision was grasped and pulled through a second open endoloop that had been placed around the stock of the first endoloop. Tightening this second ligature enabled approximation of both edges of the incision and provided complete closure of the gastrotomy (Fig. 1). Patency of the incision was evaluated by using intraabdominal pressure monitoring after air insufflation in the stomach.

Postoperative period All pigs recovered well after extubation and were placed in an animal facility where they were evaluated daily for signs of complications. They were fed standard swine chow starting on the first postoperative day. After a follow-up period of 1 to 3 weeks, they were killed by using the above-mentioned anesthetic technique followed by the application of KCl (30 –50 mL). After endoscopic evaluation of the closure site, thorough exploration of the peritoneal cavity for signs of complications was performed. Pressure leak tests in surgically removed stomachs were performed. Briefly, a T-shaped tube was used with one end placed through the esophageal remnant into the stomach, a second end was plugged into a manometer, and the third end was placed in a 4-L reservoir of water. The stomach was filled with water, the closure site was visually monitored for leakage, and pressures were continuously recorded. Finally, samples for histological examination of the closure site were taken.

RESULTS Access into the peritoneal cavity was gained in all animals without any complications. Peritoneoscopy did not reveal any injuries to adjacent organs. The fallopian tubes were identified in all the animals, and a unilateral salpinVolume 71, No. 4 : 2010 GASTROINTESTINAL ENDOSCOPY

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Figure 1. Schematic illustration of the double-endoloop closure technique. A, Gastric incision. B, Delivery of the first endoloop using a grasper. C, Delivery of second endoloop using a grasper. D, Polyp-like lesion with incision on top enclosed by 2 endoloops.

gectomy was performed (on the left side in 5 animals, on the right side in 5 animals). The gastric incision site closure was successfully performed by applying 2 endoloop ligatures in all animals with a median procedure time of 17 minutes (range 13-25 minutes, interquartile range 6). The double-endoloop technique resulted in the formation of a polyp-like lesion with the incision at the top of the formed structure (Figs. 1 and 2). In all cases, the endoscopic appearance of a complete closure was achieved. At the conclusion of the procedure, we observed full distention of the stomach with air insufflation in all cases. After desufflation of carbon dioxide from the peritoneal cavity, we insufflated air for at least 1 minute with the endoscope still in the stomach and did not observe an increase in the intra-abdominal pressure in any of the animals. The animals recovered well and started a regular diet on the first postoperative day. During the follow-up periods of 1 week (4 animals), 2 weeks (4 animals), and 3 weeks (2 animals), there were no clinical signs suggestive of a complication. The mean weight gain of the animals at 3 weeks was 21 kg (range 19.5–22.5). 808 GASTROINTESTINAL ENDOSCOPY

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Endoscopic examination before necropsy revealed normal-appearing stomachs that were easily fully distended with insufflation in all the animals, and the site of closure appeared well healed without signs of gross ulceration or inflammation (Fig. 3). The surgical site was identified by the presence of protruding mucosa, endoloops, or a superficial mucosal defect. The endoloops were still in place in 5 of the 10 animals (in 3 animals at 1 week, in 2 animals at 2 weeks, and in no animals at 3 weeks). At necropsy, there were no signs of organ damage or inflammation within the peritoneal cavity. Both the serosal and mucosal sides of the incision closure appeared well healed in all cases. Small adhesions were found in 5 of the 10 animals on the serosal side of the closure site. The removed stomachs from the 2 animals that survived 3 weeks were subjected to pressure leak tests. The gastrotomy sites remained intact under pressures exceeding 160 mm Hg. Histopathological examination of the excised closure sites confirmed complete closure in all of the animals (Fig. 3). In some animals, there was focal superficial mucosal erosion with inflammatory cells (mixed inwww.giejournal.org

Hucl et al

Novel double-endoloop technique for NOTES gastric access site closure

Figure 2. Double-endoloop technique of incision closure. A, Delivery of first endoloop. B, First endoloop in place. C, Delivery of second endoloop. D, Closed incision site by 2 endoloops.

flammatory cell population) that was restricted to the immediate site of closure. No bacteria, fungi, or abscesses were identified.

DISCUSSION NOTES is an experimental surgical approach limited mostly to animal procedures thus far. Although a variety of NOTES procedures are technically feasible, such as tubal ligation, cholecystectomy, gastrectomy, pancreatectomy, colectomy, and nephrectomy,4 efficient and safe closure of the access site remains one of the key obstacles limiting the application of NOTES in human patients. Safe closure has been targeted as a major priority of NOTES research by experts.10 A wide variety of closure techniques and devices has been described. Specific devices include the Eagle Claw,11 Gprox,12 Plicator,13 and staplers.14 These devices tend to be difficult to use, unavailable, or expensive.5,6,11-14 Deployment of tissue anchors, such as T-tags and T-bars,15,16 requires a transmural puncture of the gastric wall and puts www.giejournal.org

adjacent organs at risk.17 Plugging devices and techniques, such as the Occluder,18 clips,3 and tunnels,19 are alternative approaches. None of these approaches have gained wide acceptance to date.3,5-6,11-19 In the current study, we describe a novel technique to close a NOTES gastric wall incision by using a doubleendoloop technique. The procedure proved to be technically simple and could be performed by using commonly available endoscopic accessories. The technique was quick, with a median closure time of less than 20 minutes. All of the study animals survived without complications. We performed air leak tests and pressure leak tests and studied the closure sites endoscopically; the closures were intact in all cases. This was confirmed histologically in a subset of pigs, revealing approximation of each gastric wall layer. Minor adhesions at the site of closure were observed in 5 of the 10 animals, and no nearby organs were injured. Furthermore, our study demonstrated reproducibility of transgastric fallopian tube ligation described by Jagannath et al.20 The use of endoloops to close NOTES incisions or perforations is not novel.21 A major problem with endVolume 71, No. 4 : 2010 GASTROINTESTINAL ENDOSCOPY

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Figure 3. Autopsy to evaluate closure. A, endoscopic view of closure. B, Cross-sectional view of closure. C, Histopathology of closure site (H&E, orig. mag. ⫻50).

oloops has been their tendency to slip over the incision site on release. Hookey et al22 reported a technique by using hemoclips as anchors. Their technique calls for the application of hemoclips on one endoloop before gastrotomy, followed by advancement of endoloops alongside the endoscope. This technique is likely to be difficult and time-consuming.23 Interestingly, the volcano-like polyp resulting from successive endoloop deployments in the study by Hookey et al is similar to the polyp-like structure observed in the current study when using the doubleendoloop technique. In an in vitro setting, postclosure leakage at pressures of approximately 50 mm Hg was noted. The leakage likely resulted from the release of the outside loop hemoclips,22 suggesting that clipping is a poor way to anchor the endoloop. Slippage of the outside endoloop was also seen in an in vivo animal study.23 810 GASTROINTESTINAL ENDOSCOPY

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Unlike the technique described by Hookey et al, the approach described in the current study uses one endoloop to anchor the second endoloop along with the polyp-like lesion that forms between the endoloop stocks. In our experience, this technique eliminates slippage. No widely accepted closure device for NOTES exists at present.6 Fritscher-Ravens6 suggested in a recent editorial that the cost of producing a new device may in fact be so high that the relatively small NOTES marketplace may not justify the investment. This highlights the value of using commonly available technology. Endoscopists’ familiarity with the instruments and accessories used in our method is an advantage and should facilitate its implementation at other centers. The simplicity of the technique is yet another advantage. In addition to NOTES closure, the technique may be used to close other defects in the wall of the www.giejournal.org

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Novel double-endoloop technique for NOTES gastric access site closure

GI tract encountered by endoscopists, such as a perforation, as long as a double-channel endoscope is available. Several limitations of our study may be noted. Only a porcine model was used, the sample size was small, and there was not a control group. Furthermore, gastric incisions in pigs can close spontaneously,3 which can call into question the relevance of porcine stomach closure studies. However, the objective of this pilot study was to examine the feasibility of a novel closure technique. In conclusion, we show that the technique of doubleendoloop closure of gastric wall NOTES incision was simple, efficacious, and safe in an animal survival study. It may also be useful in cases of perforation closures in intraluminal GI endoscopy.

9. Kantsevoy SV, Jagannath SB, Niiyama H, et al. A novel safe approach to the peritoneal cavity for per-oral transgastric endoscopic procedures. Gastrointest Endosc 2007;65:497-500. 10. Rattner D, Kalloo A; ASGE/SAGES Working Group. ASGE/SAGES Working Group on Natural Orifice Translumenal Endoscopic Surgery. October 2005. Surg Endosc 2006;20:329-33. 11. Chiu PW, Lau JY, Ng EK, et al. Closure of a gastrotomy after transgastric tubal ligation by using the Eagle Claw VII: a survival experiment in a porcine model (with video). Gastrointest Endosc 2008;68:554-9. 12. Mellinger JD, MacFadyen BV, Kozarek RA, et al. Initial experience with a novel endoscopic device allowing intragastric manipulation and plication. Surg Endosc 2007;21:1002-5. 13. von Renteln D, Eickhoff A, Kaehler G, et al. Endoscopic closure of the natural orifice transluminal endoscopic surgery (NOTES) access site to the peritoneal cavity by means of transmural resorbable sutures: an animal survival study. Endoscopy 2009;41:154-9. 14. Meireles OR, Kantsevoy SV, Assumpcao LR, et al. Reliable gastric closure after natural orifice translumenal endoscopic surgery (NOTES) using a novel automated flexible stapling device. Surg Endosc 2008;22:160913. 15. Bergström M, Swain P, Park PO. Early clinical experience with a new flexible endoscopic suturing method for natural orifice transluminal endoscopic surgery and intraluminal endosurgery (with videos). Gastrointest Endosc 2008;67:528-33. 16. Sumiyama K, Gostout CJ, Rajan E, et al. Endoscopic full-thickness closure of large gastric perforations by use of tissue anchors. Gastrointest Endosc 2007;65:134-9. 17. Sumiyama K, Gostout CJ, Rajan E, et al. Submucosal endoscopy with mucosal flap safety valve. Gastrointest Endosc 2007;65:688-94. 18. Perretta S, Sereno S, Forgione A, et al. A new method to close the gastrotomy by using a cardiac septal occluder: long-term survival study in a porcine model. Gastrointest Endosc 2007;66:809-13. 19. Pauli EM, Moyer MT, Haluck RS, et al. Self-approximating transluminal access technique for natural orifice transluminal endoscopic surgery: a porcine survival study (with video). Gastrointest Endosc 2008;67:690-7. 20. Jagannath SB, Kantsevoy SV, Vaughn CA, et al. Peroral transgastric endoscopic ligation of fallopian tubes with long-term survival in a porcine model. Gastrointest Endosc 2005;61:449-53. 21. Celestino C, Harz C, Decaestecker J, et al. Endoscopic treatment of an iatrogenic perforation of the colon by using endoloop. Gastrointest Endosc 2006;64:653-4. 22. Hookey LC, Khokhotva V, Bielawska B, et al. The Queen’s closure: a novel technique for closure of endoscopic gastrotomy for natural-orifice transluminal endoscopic surgery. Endoscopy 2009;4:149-53. 23. Hookey LC, Bielawska B, Samis A, et al. A reliable and safe gastrotomy closure technique assessed in a porcine survival model pilot study: success of the Queen’s closure. Endoscopy 2009;41:493-7.

ACKNOWLEDGMENT The authors thank Olympus Germany and Olympus Czech Republic for providing technical support and Dr. J. M. Winter (Memorial Sloan-Kettering Cancer Center, New York, NY) for critical revision of the manuscript. REFERENCES 1. Zacks SL, Sandler RS, Rutledge R, et al. A population-based cohort study comparing laparoscopic cholecystectomy and open cholecystectomy. Am J Gastroenterol 2002;334-40. 2. Muckleroy SK, Ratzer ER, Fenoglio ME. Laparoscopic colon surgery for benign disease: a comparison to open surgery. JSLS 1999;3:33-7. 3. Kalloo AN, Singh VK, Jagannath SB, et al. Flexible transgastric peritoneoscopy: a novel approach to diagnostic and therapeutic interventions in the peritoneal cavity. Gastrointest Endosc 2004;60:114-7. 4. Giday SA, Kantsevoy SV, Kalloo AN. Current status of natural orifice translumenal surgery. Gastrointest Endosc Clin N Am 2007;17:595-604. 5. Voermans RP, Worm AM, van Berge Henegouwen MI, et al. In vitro comparison and evaluation of seven gastric closure modalities for natural orifice transluminal endoscopic surgery (NOTES). Endoscopy 2008;40: 595-601. 6. Fritscher-Ravens A. A market for gastric NOTES closure: which path should we take? Endoscopy 2009;41:160-1. 7. Zorron R, Maggioni LC, Pombo L, et al. NOTES transvaginal cholecystectomy: preliminary clinical application. Surg Endosc 2008;22:542-7. 8. Marescaux J, Dallemagne B, Perretta S, et al. Surgery without scars: report of transluminal cholecystectomy in a human being. Arch Surg 2007;142:823-6.

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