- Email: [email protected]
Flexible transgastric peritoneoscopy and liver biopsy: a feasibility study in human beings (with videos)
ORIGINAL ARTICLE: Clinical Endoscopy
Flexible transgastric peritoneoscopy and liver biopsy: a feasibility study in human beings (with videos) Kimberley Steele, MD, Michael A. Schweitzer, MD, Jerome Lyn-Sue, MD, Sergey V. Kantsevoy, MD, PhD Baltimore, Maryland, USA
Background: Multiple studies have demonstrated the feasibility of natural orifice transluminal endoscopic surgery in animal models. Objective: To determine the feasibility of transgastric peritoneoscopy and liver biopsy in human beings. Setting: Our institutional review board approved the procedures in the operating room with the patients under general anesthesia. Design and Interventions: During laparoscopic gastric bypass surgery a flexible endoscope was introduced into the peritoneal cavity through the gastric-wall incision. A peritoneoscopy with a liver biopsy was performed, then the flexible endoscope was withdrawn into the stomach, and gastric bypass surgery was completed laparoscopically. Patients: Three patients who were morbidly obese (mean weight 115.22 9.07 kg [254 20 lb]). Main Outcome Measurements: The ability to navigate a flexible endoscope inside the peritoneal cavity, to visualize the intra-abdominal organs, and to perform a liver biopsy without laparoscopic assistance. Results: It was very easy to navigate the flexible endoscope inside the abdomen by using torque, advancement, and withdrawal of the endoscopic shaft, as well as by movement of the endoscope tip. The flexible endoscope provided an excellent view and adequate illumination of the peritoneal cavity. The orientation of the flexible endoscope inside the peritoneal cavity was technically easy, even in the retroflex position. Systematic visualization of the liver, the spleen, the omentum, and the small and large intestine was easily achieved through the flexible endoscope without laparoscopic assistance. A liver biopsy was successfully completed in all cases by obtaining adequate tissue samples for histologic examination. Limitation: This was a pilot feasibility study. Conclusions: Transgastric flexible endoscopic peritoneoscopy in human beings is technically feasible, simple, and can become a valuable tool that complements and facilitates laparoscopic interventions inside the peritoneal cavity. (Gastrointest Endosc 2008;68:61-6.)
Our group previously demonstrated the technical feasibility of the transgastric approach to the peritoneal cavity in a porcine model.1 Since that time, transgastric gastrojejunostomy, cholecystectomy, splenectomy, tubal ligation and resection, and diaphragmal pacing, as well as transcolonic and transvesical peritoneoscopy and cholecystectomy, have been reported, and the concept of natural orifice transluminal endoscopic surgery (NOTES) has been introduced.2-30
However, all these studies were done only on animal models, followed by an abstract and several press releases of human laparoscopically assisted transvaginal and transgastric cholecystectomies, with a single published case report that described human transgastric PEG-tube rescue.31-34 There are currently no studies published as full-length, peer-reviewed articles that explored NOTES procedures in human beings. The aim of the current study was to determine the feasibility of transgastric peritoneoscopy and a liver biopsy in human beings.
Abbreviations: BMI, body mass index; NOTES, natural orifice transluminal endoscopic surgery.
PATIENTS AND METHODS
Copyright ª 2008 by the American Society for Gastrointestinal Endoscopy 0016-5107/$32.00 doi:10.1016/j.gie.2007.09.040
The study was approved by the Johns Hopkins Institutional Review Board. Informed consent was obtained from
www.giejournal.org
Volume 68, No. 1 : 2008 GASTROINTESTINAL ENDOSCOPY 61
Flexible transgastric peritoneoscopy and liver biopsy
3 patients who were morbidly obese (mean weight 115.22 9.07 kg [254 20 lb] and a body mass index [BMI] of 40 2) who were scheduled to undergo laparoscopic gastric bypass and were enrolled into the study. The patients were restricted to no food by mouth for 8 hours before the procedure. All the patients were given a preoperative dose of a broad spectrum intravenous antibiotic within 1 hour before the first skin incision. The laparoscopic interventions were performed in the operating room, with the patient under general anesthesia with endotracheal intubation. A pneumoperitoneum with carbon dioxide was created by using the High-Flow laparoscopic insufflator (Stryker Corp, Kalamazoo, Mich) with a preset intra-abdominal pressure of 15 mm Hg. Two 5-mm trocars (right and left upper quadrants) and two 12-mm trocars (left upper quadrant and supraumbilical area) were inserted into the peritoneal cavity through the anterior abdominal wall. By using previously described laparoscopic techniques, the Roux limb of the small bowel was constructed, followed by division of the stomach into a 20-mL upper gastric pouch.35 After dividing the stomach, a transmural gastric-wall incision for a subsequent gastrojejunostomy was made on the anterior wall of the stomach by using an extra-long US shears (Auto Sonix XL; United States Surgical, Norwalk, Conn). A clean and disinfected forward-viewing flexible upper endoscope (GIF-160; Olympus America Inc, Center Valley, Pa) was then advanced through the gastric-wall opening into the peritoneal cavity. A liver biopsy was performed by using a regular endoscopic forceps (FB-24K-1; Olympus America Inc, Center Valley, Pa) through the biopsy channel of the flexible endoscope to obtain a specimen for histologic evaluation and grading of steatohepatitis. After the liver biopsy, the peritoneal cavity was systematically explored through the flexible endoscope with a laparoscopic light source switched on and off. After the peritoneoscopy, the endoscope was withdrawn into the stomach. The gastric-wall incision used for the transgastric peritoneoscopy was then connected with the Roux limb to form an end-to-side stapled gastrojejunal anastomosis reinforced by an outer layer of running sutures (the 2-layer gastrojejunostomy technique).36 After the gastric bypass surgery was completed, the trocars were removed, the abdominal-wall incisions were sutured, and tissue adhesive (Indermil; Tyco Healthcare, Norwalk, Conn) was applied. The patients recovered from general anesthesia and were transferred to their room for regular postsurgical care. The antibiotic was continued for 24 hours. All the patients were observed for 1 month by a bariatric nurse practitioner, with particular attention for signs and symptoms of bleeding, infection, leakage, or other postoperative complications.
RESULTS In all 3 patients, the flexible endoscope was passed through the gastric-wall opening into the peritoneal cavity 62 GASTROINTESTINAL ENDOSCOPY Volume 68, No. 1 : 2008
Steele et al
Capsule Summary What is already known on this topic d
Natural orifice transluminal endoscopic surgical procedures do not require incision of the anterior abdominal wall and so would be attractive in patients who are morbidly obese, but all previous research has used animal models.
What this study adds to our knowledge d
Flexible transgastric peritoneoscopy and liver biopsy performed during laparoscopic gastric bypass surgery in 3 patients who were morbidly obese did not interfere with a gastrojejunal anastomosis creation, did not result in any local or systemic complications during or after the procedure, and prolonged the time of bypass by only 4 to 6 minutes.
without any problems (Fig. 1). It was very easy to navigate the flexible endoscope inside the abdomen by using torque, advancement, and withdrawal of the endoscopic shaft, as well as up, down, right, and left movements of its tip (Video 1, available online at www.giejournal.org). The flexible endoscope provided an excellent view and adequate illumination of the peritoneal cavity, even when the laparoscopic light source was switched off (Video 2, available online at www.giejournal.org). A laparoscopic automated insufflator provided an adequate pneumoperitoneum. We did not have to use any additional air insufflation through the flexible endoscope during the transgastric peritoneoscopy and liver biopsy. We used imprints from the pressure by the surgeon’s finger on the abdominal wall (right and left upper quadrant, periumbilical area, etc) and anatomical landmarks (liver, falciform ligament, small bowel, and omentum) to facilitate the orientation of the flexible endoscope and to navigate it inside the peritoneal cavity. Systematic evaluation of the liver (Fig. 2), the epigastric area (Fig. 3), the small intestine (Fig. 4), and the omentum (Fig. 5) was achieved through the flexible endoscope, without any laparoscopic assistance (a laparoscopic liver retractor was used to facilitate sleeve gastrectomy and was not removed or repositioned during the transgastric peritoneoscopy). We were able to visualize segments II, III, IVb, V, and, partially, segment VI. Right lateral segments (VI and VII), superior segments (IVa and VIII), and segment I of the liver were not visualized through the flexible endoscope. All laparoscopic trocars and accessories inside the peritoneal cavity were effortlessly visualized in their entire length through the flexible endoscope. A liver biopsy was performed from segments II, III, and IVb by obtaining adequate tissue samples for histologic examination (Fig. 6; Videos 3 and 4, available online at www.giejournal.org). There was only minor bleeding from www.giejournal.org
Steele et al
Flexible transgastric peritoneoscopy and liver biopsy
Figure 1. Laparoscopic view of the flexible endoscope entering the peritoneal cavity through the gastric-wall opening.
Figure 3. Transgastric peritoneoscopy: retroflex panoramic view of the epigastric area through the flexible endoscope.
Figure 2. Transgastric peritoneoscopy: view of the liver through the flexible endoscope.
Figure 4. Transgastric peritoneoscopy: view of the small intestine through the flexible endoscope.
the liver biopsy sites. This bleeding did not require any local hemostatic measures; all patients were observed and bleeding stopped spontaneously after 2 minutes. A histologic examination of the biopsy specimens demonstrated moderate periportal inflammation and minimal steatosis, without an increase in intralobular fibrosis (Fig. 7A and B). Exploration of the peritoneal cavity with a flexible endoscope and a liver biopsy took 2.1 minutes in the first patient, 4.3 minutes in the second patient, and 6.0 minutes in the third patient (average [GSD] time 4.1 1.9 minutes). In all cases, laparoscopic creation of a gastrojejunal bypass was not affected by a previous transgastric peritoneoscopy. All procedures were successfully completed laparoscopically. The postoperative period in all patients was uneventful, without any local or systemic complications. None of the patients exhibited any signs or symptoms of intra-abdominal or trocar wound infection during a 1-month follow-up after the procedure.
DISCUSSION
www.giejournal.org
The concept of NOTES uses a transluminal approach to the peritoneal cavity, without the need for abdominal-wall incisions.28-30 Current NOTES knowledge is based on multiple abstracts plus 27 full-length peer-reviewed articles that summarize a total of 202 animal experiments, as well as abstracts or press releases that announced human transvaginal and transgastric cholecystectomies, and 1 published case report of a human transgastric PEG-rescue procedure.1-27,31-34 Our study was designed to determine the feasibility of the transgastric approach for systematic exploration of the peritoneal cavity and liver biopsies by using a flexible endoscope. NOTES procedures do not require an incision of the anterior abdominal wall and, therefore, appear especially attractive for patients who are morbidly obese. For this reason, we chose, for our study, only patients Volume 68, No. 1 : 2008 GASTROINTESTINAL ENDOSCOPY 63
Flexible transgastric peritoneoscopy and liver biopsy
Steele et al
Figure 5. Transgastric peritoneoscopy: view of the omentum through the flexible endoscope.
Figure 6. Transgastric liver biopsy: view through the flexible endoscope.
Figure 7. Histologic examination of the specimen obtained by a transgastric liver biopsy, showing moderate periportal inflammation and minimal steatosis, without an increase in intralobular fibrosis. A, Low-power magnification view (H&E, orig. mag. 200). B, High-power magnification view (H&E, orig. mag. 400).
who were morbidly obese, with a mean weight of 115.22 9.07 kg (254 20 lb) and BMI 40 2, who were undergoing laparoscopic gastric bypass surgery. In a previously reported abstract, Hazey et al37 demonstrated that a laparoscopic gastric bypass in which they made a gastric-wall incision and passed an anvil through the gastrotomy into the peritoneal cavity did not cause any clinically significant peritoneal contamination and did not lead to any septic intra-abdominal or systemic complications. Based on these results, we went to the next step and advanced a flexible endoscope through the gastric-wall incision into the peritoneal cavity to perform a NOTES peritoneoscopy and a liver biopsy. Even in these patients with large depositions of fat inside the peritoneal cavity (the falciform ligament, omentum, bowel mesentery, etc), a flexible endoscope provided an excellent view of the intra-abdominal organs, even when a laparoscopic light source was switched off. The navigation of the flexible endoscope was easily achieved with regular maneuvers used during the intraluminal
flexible endoscopy: torque, advance and withdrawal of the shaft, and movements of the tip of the endoscope up, down, right, and left. Several experts raised concerns regarding potential difficulties of orientation of the flexible endoscope inside the peritoneal cavity.28 In our previously reported animal hybrid procedures, laparoscopic observation simplified the orientation of the flexible endoscope inside the peritoneal cavity.18 During our human NOTES procedures, we used imprints from the pressure of the surgeon’s finger on the abdominal wall and intraperitoneal anatomical landmarks to facilitate the orientation and navigation of the flexible endoscope inside the peritoneal cavity. Visualization of the intra-abdominal organs, laparoscopic trocars, and accessories inside the peritoneal cavity was effortless and unrestricted. The transgastric peritoneal exploration and liver biopsy were quick and easy to perform, prolonging the time of the laparoscopic gastric bypass by only 4 to 6 minutes. It also provided important information about liver architecture and liver damage caused by the preexisting morbid
64 GASTROINTESTINAL ENDOSCOPY Volume 68, No. 1 : 2008
www.giejournal.org
Steele et al
obesity. A transgastric peritoneoscopy did not interfere with gastrojejunal anastomosis creation and did not result in any local or systemic complications during the laparoscopic intervention or during postoperative period. The main limitation of our study was that it was only a pilot study and could not address all the questions related to NOTES procedures in human beings.38-42 For example, we did not design our study to determine how to enter the peritoneal cavity without injury to the adjacent organs or to develop closure for a gastric-wall incision. In our currently reported study, the location for a transgastric entrance into the peritoneal cavity was determined by the position of a subsequent gastrojejunal anastomosis and was not optimal for a transgastric peritoneoscopy; in currently reported animal experiments, the entrance into the peritoneal cavity was usually made through the anterior wall at the junction of the body and the antrum of the stomach.1,2 We also made a gastric-wall incision laparoscopically and did not close it but instead used it for a subsequent gastrojejunal anastomosis. We consciously simplified the study design to demonstrate the feasibility of NOTES procedures in human beings. We are now planning a larger trial to explore, in detail, the safety, gastric closure techniques, and other issues related to human NOTES procedures. In conclusion, a transgastric flexible endoscopic peritoneoscopy in human beings is technically feasible and simple, and can become a valuable tool that complements and facilitates laparoscopic interventions inside the peritoneal cavity.
DISCLOSURE The following authors report that they have no disclosures relevant to this publication: K. Steele, M. A. Schweitzer, J. Lyn-Sue. The following author has disclosed an actual or potential conflict: S. Kantsevoy is an equity holder in Apollo Endosurgery Inc, Austin, Texas.
REFERENCES 1. 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. 2. Kantsevoy SV, Jagannath SB, Niiyama H, et al. Endoscopic gastrojejunostomy with survival in a porcine model. Gastrointest Endosc 2005;62:287-92. 3. Park PO, Bergstrom M, Ikeda K, et al. Experimental studies of transgastric gallbladder surgery: cholecystectomy and cholecystogastric anastomosis (videos). Gastrointest Endosc 2005;61:601-6. 4. Swanstrom LL, Kozarek R, Pasricha PJ, et al. Development of a new access device for transgastric surgery. J Gastrointest Surg 2005;9: 1129-36, discussion 1136–7. 5. Bergstrom M, Ikeda K, Swain P, et al. Transgastric anastomosis by using flexible endoscopy in a porcine model (with video). Gastrointest Endosc 2006;63:307-12.
www.giejournal.org
Flexible transgastric peritoneoscopy and liver biopsy 6. 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. 7. Wagh MS, Merrifield BF, Thompson CC. Endoscopic transgastric abdominal exploration and organ resection: initial experience in a porcine model. Clin Gastroenterol Hepatol 2005;3:892-6. 8. Kantsevoy SV, Hu B, Jagannath SB, et al. Transgastric endoscopic splenectomy: is it possible? Surg Endosc 2006;20:522-5. 9. Wagh MS, Merrifield BF, Thompson CC. Survival studies after endoscopic transgastric oophorectomy and tubectomy in a porcine model. Gastrointest Endosc 2006;63:473-8. 10. Merrifield BF, Wagh MS, Thompson CC. Peroral transgastric organ resection: a feasibility study in pigs. Gastrointest Endosc 2006;63:693-7. 11. Fritscher-Ravens A, Mosse CA, Ikeda K, et al. Endoscopic transgastric lymphadenectomy by using EUS for selection and guidance. Gastrointest Endosc 2006;63:302-6. 12. Sumiyama K, Gostout CJ, Rajan E, et al. Pilot study of the porcine uterine horn as an in vivo appendicitis model for development of endoscopic transgastric appendectomy. Gastrointest Endosc 2006;64:808-12. 13. Lima E, Rolanda C, Pego JM, et al. Transvesical endoscopic peritoneoscopy: a novel 5 mm port for intra-abdominal scarless surgery. J Urol 2006;176:802-5. 14. Kantsevoy SV, Niiyama H, Jagannath SB, et al. The endoscopic transilluminator: an endoscopic device for identification of the proximal jejunum for transgastric endoscopic gastrojejunostomy. Gastrointest Endosc 2006;63:1055-8. 15. Pai RD, Fong DG, Bundga ME, et al. Transcolonic endoscopic cholecystectomy: a NOTES survival study in a porcine model (with video). Gastrointest Endosc 2006;64:428-34. 16. Rolanda C, Lima E, Pego JM, et al. Third-generation cholecystectomy by natural orifices: transgastric and transvesical combined approach (with video). Gastrointest Endosc 2007;65:111-7. 17. Onders R, McGee MF, Marks J, et al. Diaphragm pacing with natural orifice transluminal endoscopic surgery: potential for difficult-to-wean intensive care unit patients. Surg Endosc 2007;21:475-9. 18. Shin S, Kantsevoy SV, Kalloo AN, et al. Hybrid minimally invasive surgery: a bridge between laparoscopic and translumenal surgery. Surg Endosc 2007;21:1450-3. 19. Fong DG, Pai RD, Thompson CC. Transcolonic endoscopic abdominal exploration: a NOTES survival study in a porcine model. Gastrointest Endosc 2007;65:312-8. 20. Ryou M, Pai R, Sauer J, et al. Evaluating an optimal gastric closure method for transgastric surgery. Surg Endosc 2007;21:677-80. 21. Meireles O, Kantsevoy SV, Kalloo AN, et al. Comparison of intraabdominal pressures using the gastroscope and laparoscope for transgastric surgery. Surg Endosc 2007;21:998-1001. 22. McGee MF, Rosen MJ, Marks J, et al. A reliable method for monitoring intraabdominal pressure during natural orifice translumenal endoscopic surgery. Surg Endosc 2007;21:672-6. 23. Kantsevoy SV, Jagannath SB, Nijiyama H, et al. A novel safe approach to the peritoneal cavity for per-oral transgastric endoscopic procedures. Gastrointest Endosc 2007;65:497-500. 24. von Delius S, Feussner H, Wilhelm D, et al. Transgastric in vivo histology in the peritoneal cavity using miniprobe-based confocal fluorescence microscopy in an acute porcine model. Endoscopy 2007;39:407-11. 25. Wilhelm D, Meining A, von Delius S, et al. An innovative, safe and sterile sigmoid access (ISSA) for NOTES. Endoscopy 2007;39:401-6. 26. Hu B, Kalloo AN, Chung SSC, et al. Per-oral transgastric endoscopic primary repair of a ventral hernia in a porcine model. Endoscopy 2007;39: 390-3. 27. Onders RP, McGee MF, Marks J, et al. Natural orifice transluminal endoscopic surgery (NOTES) as a diagnostic tool in the intensive care unit. Surg Endosc 2007;21:681-3. 28. American Society for Gastrointestinal Endoscopy/SAGES Working Group, Rattner D, Kalloo A. ASGE/SAGES Working Group on Natural Orifice Translumenal Endoscopic Surgery. October 2005. Surg Endosc 2006;20:329-33.
Volume 68, No. 1 : 2008 GASTROINTESTINAL ENDOSCOPY 65
Flexible transgastric peritoneoscopy and liver biopsy 29. Swain CP. A justification for NOTES: natural orifice translumenal endosurgery. Gastrointest Endosc 2007;66:514-6. 30. Rattner D, Hawes RH. NOTES: gathering momentum. Gastrointest Endosc 2006;63:838-9. 31. Bessler M, Stevens P, Milone L, et al. Transvaginal cholecystectomy, laparoscopically assisted, for gallstones, a human case. SAGES 2007 final program 2007:ET017. 32. WeBSurg’s World Virtual University July 2007. Available at: http://www.websurg.com/notes/experts/index.php. Accessed August 1, 2007. 33. USGI Medical. News June 25 2007. Available at: http://www.usgimedical. com. Accessed August 1, 2007. 34. Marks JM, Ponsky JL, Pearl JP, et al. PEG ‘‘rescue’’: a practical NOTES technique. Surg Endosc 2007;21:816-9. 35. Schweitzer MA, Demaria EJ, Sugerman HA. Laparoscopic Roux-en-Y gastric bypass procedure. Surg Rounds 2000;23:371-80. 36. Schweitzer MA, Lidor A, Magnuson TH. A zero leak rate in 251 consecutive laparoscopic gastric bypass operations using a two-layer gastrojejunostomy technique. J Laparoendosc Adv Surg Tech 2006;16:83-7. 37. Hazey JW, Needleman BJ, Melvin WS, et al. Transgastric instrumentations and bacterial contamination of the peritoneal cavity. SAGES 2007 final program 2007:S044.
66 GASTROINTESTINAL ENDOSCOPY Volume 68, No. 1 : 2008
Steele et al 38. Ponsky JL. Gastroenterologists as surgeons: what they need to know [abstract]. Gastrointest Endosc 2005;61:454. 39. Hochberger J, Lamade W. Transgastric surgery in the abdomen: the dawn of a new era? Gastrointest Endosc 2005;62:293-6. 40. Lamade W, Hochberger J. Transgastric surgery: avoiding pitfalls in the development of a new technique. Gastrointest Endosc 2006;63: 698-700. 41. Fritscher-Ravens A. Transgastric endoscopy: a new fashion, a new excitement! Endoscopy 2007;39:161-7. 42. Reddy DN, Rao GV. Transgastric approach to the peritoneal cavity: are we on the right track? Gastrointest Endosc 2007;65:501-2.
Received August 2, 2007. Accepted September 4, 2007. Current affiliations: Department of Surgery (K.S., M.A.S., J.L.-S.), Division of Gastroenterology (S.V.K.), Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. Reprint requests: Sergey V. Kantsevoy, MD, Division of Gastroenterology, Johns Hopkins Hospital, 1830 East Monument St, Rm 423, Baltimore, MD 21205.
www.giejournal.org
Flexible transgastric peritoneoscopy and liver biopsy: a feasibility study in human beings (with videos) Kimberley Steele, MD, Michael A. Schweitzer, MD, Jerome Lyn-Sue, MD, Sergey V. Kantsevoy, MD, PhD Baltimore, Maryland, USA
Background: Multiple studies have demonstrated the feasibility of natural orifice transluminal endoscopic surgery in animal models. Objective: To determine the feasibility of transgastric peritoneoscopy and liver biopsy in human beings. Setting: Our institutional review board approved the procedures in the operating room with the patients under general anesthesia. Design and Interventions: During laparoscopic gastric bypass surgery a flexible endoscope was introduced into the peritoneal cavity through the gastric-wall incision. A peritoneoscopy with a liver biopsy was performed, then the flexible endoscope was withdrawn into the stomach, and gastric bypass surgery was completed laparoscopically. Patients: Three patients who were morbidly obese (mean weight 115.22 9.07 kg [254 20 lb]). Main Outcome Measurements: The ability to navigate a flexible endoscope inside the peritoneal cavity, to visualize the intra-abdominal organs, and to perform a liver biopsy without laparoscopic assistance. Results: It was very easy to navigate the flexible endoscope inside the abdomen by using torque, advancement, and withdrawal of the endoscopic shaft, as well as by movement of the endoscope tip. The flexible endoscope provided an excellent view and adequate illumination of the peritoneal cavity. The orientation of the flexible endoscope inside the peritoneal cavity was technically easy, even in the retroflex position. Systematic visualization of the liver, the spleen, the omentum, and the small and large intestine was easily achieved through the flexible endoscope without laparoscopic assistance. A liver biopsy was successfully completed in all cases by obtaining adequate tissue samples for histologic examination. Limitation: This was a pilot feasibility study. Conclusions: Transgastric flexible endoscopic peritoneoscopy in human beings is technically feasible, simple, and can become a valuable tool that complements and facilitates laparoscopic interventions inside the peritoneal cavity. (Gastrointest Endosc 2008;68:61-6.)
Our group previously demonstrated the technical feasibility of the transgastric approach to the peritoneal cavity in a porcine model.1 Since that time, transgastric gastrojejunostomy, cholecystectomy, splenectomy, tubal ligation and resection, and diaphragmal pacing, as well as transcolonic and transvesical peritoneoscopy and cholecystectomy, have been reported, and the concept of natural orifice transluminal endoscopic surgery (NOTES) has been introduced.2-30
However, all these studies were done only on animal models, followed by an abstract and several press releases of human laparoscopically assisted transvaginal and transgastric cholecystectomies, with a single published case report that described human transgastric PEG-tube rescue.31-34 There are currently no studies published as full-length, peer-reviewed articles that explored NOTES procedures in human beings. The aim of the current study was to determine the feasibility of transgastric peritoneoscopy and a liver biopsy in human beings.
Abbreviations: BMI, body mass index; NOTES, natural orifice transluminal endoscopic surgery.
PATIENTS AND METHODS
Copyright ª 2008 by the American Society for Gastrointestinal Endoscopy 0016-5107/$32.00 doi:10.1016/j.gie.2007.09.040
The study was approved by the Johns Hopkins Institutional Review Board. Informed consent was obtained from
www.giejournal.org
Volume 68, No. 1 : 2008 GASTROINTESTINAL ENDOSCOPY 61
Flexible transgastric peritoneoscopy and liver biopsy
3 patients who were morbidly obese (mean weight 115.22 9.07 kg [254 20 lb] and a body mass index [BMI] of 40 2) who were scheduled to undergo laparoscopic gastric bypass and were enrolled into the study. The patients were restricted to no food by mouth for 8 hours before the procedure. All the patients were given a preoperative dose of a broad spectrum intravenous antibiotic within 1 hour before the first skin incision. The laparoscopic interventions were performed in the operating room, with the patient under general anesthesia with endotracheal intubation. A pneumoperitoneum with carbon dioxide was created by using the High-Flow laparoscopic insufflator (Stryker Corp, Kalamazoo, Mich) with a preset intra-abdominal pressure of 15 mm Hg. Two 5-mm trocars (right and left upper quadrants) and two 12-mm trocars (left upper quadrant and supraumbilical area) were inserted into the peritoneal cavity through the anterior abdominal wall. By using previously described laparoscopic techniques, the Roux limb of the small bowel was constructed, followed by division of the stomach into a 20-mL upper gastric pouch.35 After dividing the stomach, a transmural gastric-wall incision for a subsequent gastrojejunostomy was made on the anterior wall of the stomach by using an extra-long US shears (Auto Sonix XL; United States Surgical, Norwalk, Conn). A clean and disinfected forward-viewing flexible upper endoscope (GIF-160; Olympus America Inc, Center Valley, Pa) was then advanced through the gastric-wall opening into the peritoneal cavity. A liver biopsy was performed by using a regular endoscopic forceps (FB-24K-1; Olympus America Inc, Center Valley, Pa) through the biopsy channel of the flexible endoscope to obtain a specimen for histologic evaluation and grading of steatohepatitis. After the liver biopsy, the peritoneal cavity was systematically explored through the flexible endoscope with a laparoscopic light source switched on and off. After the peritoneoscopy, the endoscope was withdrawn into the stomach. The gastric-wall incision used for the transgastric peritoneoscopy was then connected with the Roux limb to form an end-to-side stapled gastrojejunal anastomosis reinforced by an outer layer of running sutures (the 2-layer gastrojejunostomy technique).36 After the gastric bypass surgery was completed, the trocars were removed, the abdominal-wall incisions were sutured, and tissue adhesive (Indermil; Tyco Healthcare, Norwalk, Conn) was applied. The patients recovered from general anesthesia and were transferred to their room for regular postsurgical care. The antibiotic was continued for 24 hours. All the patients were observed for 1 month by a bariatric nurse practitioner, with particular attention for signs and symptoms of bleeding, infection, leakage, or other postoperative complications.
RESULTS In all 3 patients, the flexible endoscope was passed through the gastric-wall opening into the peritoneal cavity 62 GASTROINTESTINAL ENDOSCOPY Volume 68, No. 1 : 2008
Steele et al
Capsule Summary What is already known on this topic d
Natural orifice transluminal endoscopic surgical procedures do not require incision of the anterior abdominal wall and so would be attractive in patients who are morbidly obese, but all previous research has used animal models.
What this study adds to our knowledge d
Flexible transgastric peritoneoscopy and liver biopsy performed during laparoscopic gastric bypass surgery in 3 patients who were morbidly obese did not interfere with a gastrojejunal anastomosis creation, did not result in any local or systemic complications during or after the procedure, and prolonged the time of bypass by only 4 to 6 minutes.
without any problems (Fig. 1). It was very easy to navigate the flexible endoscope inside the abdomen by using torque, advancement, and withdrawal of the endoscopic shaft, as well as up, down, right, and left movements of its tip (Video 1, available online at www.giejournal.org). The flexible endoscope provided an excellent view and adequate illumination of the peritoneal cavity, even when the laparoscopic light source was switched off (Video 2, available online at www.giejournal.org). A laparoscopic automated insufflator provided an adequate pneumoperitoneum. We did not have to use any additional air insufflation through the flexible endoscope during the transgastric peritoneoscopy and liver biopsy. We used imprints from the pressure by the surgeon’s finger on the abdominal wall (right and left upper quadrant, periumbilical area, etc) and anatomical landmarks (liver, falciform ligament, small bowel, and omentum) to facilitate the orientation of the flexible endoscope and to navigate it inside the peritoneal cavity. Systematic evaluation of the liver (Fig. 2), the epigastric area (Fig. 3), the small intestine (Fig. 4), and the omentum (Fig. 5) was achieved through the flexible endoscope, without any laparoscopic assistance (a laparoscopic liver retractor was used to facilitate sleeve gastrectomy and was not removed or repositioned during the transgastric peritoneoscopy). We were able to visualize segments II, III, IVb, V, and, partially, segment VI. Right lateral segments (VI and VII), superior segments (IVa and VIII), and segment I of the liver were not visualized through the flexible endoscope. All laparoscopic trocars and accessories inside the peritoneal cavity were effortlessly visualized in their entire length through the flexible endoscope. A liver biopsy was performed from segments II, III, and IVb by obtaining adequate tissue samples for histologic examination (Fig. 6; Videos 3 and 4, available online at www.giejournal.org). There was only minor bleeding from www.giejournal.org
Steele et al
Flexible transgastric peritoneoscopy and liver biopsy
Figure 1. Laparoscopic view of the flexible endoscope entering the peritoneal cavity through the gastric-wall opening.
Figure 3. Transgastric peritoneoscopy: retroflex panoramic view of the epigastric area through the flexible endoscope.
Figure 2. Transgastric peritoneoscopy: view of the liver through the flexible endoscope.
Figure 4. Transgastric peritoneoscopy: view of the small intestine through the flexible endoscope.
the liver biopsy sites. This bleeding did not require any local hemostatic measures; all patients were observed and bleeding stopped spontaneously after 2 minutes. A histologic examination of the biopsy specimens demonstrated moderate periportal inflammation and minimal steatosis, without an increase in intralobular fibrosis (Fig. 7A and B). Exploration of the peritoneal cavity with a flexible endoscope and a liver biopsy took 2.1 minutes in the first patient, 4.3 minutes in the second patient, and 6.0 minutes in the third patient (average [GSD] time 4.1 1.9 minutes). In all cases, laparoscopic creation of a gastrojejunal bypass was not affected by a previous transgastric peritoneoscopy. All procedures were successfully completed laparoscopically. The postoperative period in all patients was uneventful, without any local or systemic complications. None of the patients exhibited any signs or symptoms of intra-abdominal or trocar wound infection during a 1-month follow-up after the procedure.
DISCUSSION
www.giejournal.org
The concept of NOTES uses a transluminal approach to the peritoneal cavity, without the need for abdominal-wall incisions.28-30 Current NOTES knowledge is based on multiple abstracts plus 27 full-length peer-reviewed articles that summarize a total of 202 animal experiments, as well as abstracts or press releases that announced human transvaginal and transgastric cholecystectomies, and 1 published case report of a human transgastric PEG-rescue procedure.1-27,31-34 Our study was designed to determine the feasibility of the transgastric approach for systematic exploration of the peritoneal cavity and liver biopsies by using a flexible endoscope. NOTES procedures do not require an incision of the anterior abdominal wall and, therefore, appear especially attractive for patients who are morbidly obese. For this reason, we chose, for our study, only patients Volume 68, No. 1 : 2008 GASTROINTESTINAL ENDOSCOPY 63
Flexible transgastric peritoneoscopy and liver biopsy
Steele et al
Figure 5. Transgastric peritoneoscopy: view of the omentum through the flexible endoscope.
Figure 6. Transgastric liver biopsy: view through the flexible endoscope.
Figure 7. Histologic examination of the specimen obtained by a transgastric liver biopsy, showing moderate periportal inflammation and minimal steatosis, without an increase in intralobular fibrosis. A, Low-power magnification view (H&E, orig. mag. 200). B, High-power magnification view (H&E, orig. mag. 400).
who were morbidly obese, with a mean weight of 115.22 9.07 kg (254 20 lb) and BMI 40 2, who were undergoing laparoscopic gastric bypass surgery. In a previously reported abstract, Hazey et al37 demonstrated that a laparoscopic gastric bypass in which they made a gastric-wall incision and passed an anvil through the gastrotomy into the peritoneal cavity did not cause any clinically significant peritoneal contamination and did not lead to any septic intra-abdominal or systemic complications. Based on these results, we went to the next step and advanced a flexible endoscope through the gastric-wall incision into the peritoneal cavity to perform a NOTES peritoneoscopy and a liver biopsy. Even in these patients with large depositions of fat inside the peritoneal cavity (the falciform ligament, omentum, bowel mesentery, etc), a flexible endoscope provided an excellent view of the intra-abdominal organs, even when a laparoscopic light source was switched off. The navigation of the flexible endoscope was easily achieved with regular maneuvers used during the intraluminal
flexible endoscopy: torque, advance and withdrawal of the shaft, and movements of the tip of the endoscope up, down, right, and left. Several experts raised concerns regarding potential difficulties of orientation of the flexible endoscope inside the peritoneal cavity.28 In our previously reported animal hybrid procedures, laparoscopic observation simplified the orientation of the flexible endoscope inside the peritoneal cavity.18 During our human NOTES procedures, we used imprints from the pressure of the surgeon’s finger on the abdominal wall and intraperitoneal anatomical landmarks to facilitate the orientation and navigation of the flexible endoscope inside the peritoneal cavity. Visualization of the intra-abdominal organs, laparoscopic trocars, and accessories inside the peritoneal cavity was effortless and unrestricted. The transgastric peritoneal exploration and liver biopsy were quick and easy to perform, prolonging the time of the laparoscopic gastric bypass by only 4 to 6 minutes. It also provided important information about liver architecture and liver damage caused by the preexisting morbid
64 GASTROINTESTINAL ENDOSCOPY Volume 68, No. 1 : 2008
www.giejournal.org
Steele et al
obesity. A transgastric peritoneoscopy did not interfere with gastrojejunal anastomosis creation and did not result in any local or systemic complications during the laparoscopic intervention or during postoperative period. The main limitation of our study was that it was only a pilot study and could not address all the questions related to NOTES procedures in human beings.38-42 For example, we did not design our study to determine how to enter the peritoneal cavity without injury to the adjacent organs or to develop closure for a gastric-wall incision. In our currently reported study, the location for a transgastric entrance into the peritoneal cavity was determined by the position of a subsequent gastrojejunal anastomosis and was not optimal for a transgastric peritoneoscopy; in currently reported animal experiments, the entrance into the peritoneal cavity was usually made through the anterior wall at the junction of the body and the antrum of the stomach.1,2 We also made a gastric-wall incision laparoscopically and did not close it but instead used it for a subsequent gastrojejunal anastomosis. We consciously simplified the study design to demonstrate the feasibility of NOTES procedures in human beings. We are now planning a larger trial to explore, in detail, the safety, gastric closure techniques, and other issues related to human NOTES procedures. In conclusion, a transgastric flexible endoscopic peritoneoscopy in human beings is technically feasible and simple, and can become a valuable tool that complements and facilitates laparoscopic interventions inside the peritoneal cavity.
DISCLOSURE The following authors report that they have no disclosures relevant to this publication: K. Steele, M. A. Schweitzer, J. Lyn-Sue. The following author has disclosed an actual or potential conflict: S. Kantsevoy is an equity holder in Apollo Endosurgery Inc, Austin, Texas.
REFERENCES 1. 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. 2. Kantsevoy SV, Jagannath SB, Niiyama H, et al. Endoscopic gastrojejunostomy with survival in a porcine model. Gastrointest Endosc 2005;62:287-92. 3. Park PO, Bergstrom M, Ikeda K, et al. Experimental studies of transgastric gallbladder surgery: cholecystectomy and cholecystogastric anastomosis (videos). Gastrointest Endosc 2005;61:601-6. 4. Swanstrom LL, Kozarek R, Pasricha PJ, et al. Development of a new access device for transgastric surgery. J Gastrointest Surg 2005;9: 1129-36, discussion 1136–7. 5. Bergstrom M, Ikeda K, Swain P, et al. Transgastric anastomosis by using flexible endoscopy in a porcine model (with video). Gastrointest Endosc 2006;63:307-12.
www.giejournal.org
Flexible transgastric peritoneoscopy and liver biopsy 6. 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. 7. Wagh MS, Merrifield BF, Thompson CC. Endoscopic transgastric abdominal exploration and organ resection: initial experience in a porcine model. Clin Gastroenterol Hepatol 2005;3:892-6. 8. Kantsevoy SV, Hu B, Jagannath SB, et al. Transgastric endoscopic splenectomy: is it possible? Surg Endosc 2006;20:522-5. 9. Wagh MS, Merrifield BF, Thompson CC. Survival studies after endoscopic transgastric oophorectomy and tubectomy in a porcine model. Gastrointest Endosc 2006;63:473-8. 10. Merrifield BF, Wagh MS, Thompson CC. Peroral transgastric organ resection: a feasibility study in pigs. Gastrointest Endosc 2006;63:693-7. 11. Fritscher-Ravens A, Mosse CA, Ikeda K, et al. Endoscopic transgastric lymphadenectomy by using EUS for selection and guidance. Gastrointest Endosc 2006;63:302-6. 12. Sumiyama K, Gostout CJ, Rajan E, et al. Pilot study of the porcine uterine horn as an in vivo appendicitis model for development of endoscopic transgastric appendectomy. Gastrointest Endosc 2006;64:808-12. 13. Lima E, Rolanda C, Pego JM, et al. Transvesical endoscopic peritoneoscopy: a novel 5 mm port for intra-abdominal scarless surgery. J Urol 2006;176:802-5. 14. Kantsevoy SV, Niiyama H, Jagannath SB, et al. The endoscopic transilluminator: an endoscopic device for identification of the proximal jejunum for transgastric endoscopic gastrojejunostomy. Gastrointest Endosc 2006;63:1055-8. 15. Pai RD, Fong DG, Bundga ME, et al. Transcolonic endoscopic cholecystectomy: a NOTES survival study in a porcine model (with video). Gastrointest Endosc 2006;64:428-34. 16. Rolanda C, Lima E, Pego JM, et al. Third-generation cholecystectomy by natural orifices: transgastric and transvesical combined approach (with video). Gastrointest Endosc 2007;65:111-7. 17. Onders R, McGee MF, Marks J, et al. Diaphragm pacing with natural orifice transluminal endoscopic surgery: potential for difficult-to-wean intensive care unit patients. Surg Endosc 2007;21:475-9. 18. Shin S, Kantsevoy SV, Kalloo AN, et al. Hybrid minimally invasive surgery: a bridge between laparoscopic and translumenal surgery. Surg Endosc 2007;21:1450-3. 19. Fong DG, Pai RD, Thompson CC. Transcolonic endoscopic abdominal exploration: a NOTES survival study in a porcine model. Gastrointest Endosc 2007;65:312-8. 20. Ryou M, Pai R, Sauer J, et al. Evaluating an optimal gastric closure method for transgastric surgery. Surg Endosc 2007;21:677-80. 21. Meireles O, Kantsevoy SV, Kalloo AN, et al. Comparison of intraabdominal pressures using the gastroscope and laparoscope for transgastric surgery. Surg Endosc 2007;21:998-1001. 22. McGee MF, Rosen MJ, Marks J, et al. A reliable method for monitoring intraabdominal pressure during natural orifice translumenal endoscopic surgery. Surg Endosc 2007;21:672-6. 23. Kantsevoy SV, Jagannath SB, Nijiyama H, et al. A novel safe approach to the peritoneal cavity for per-oral transgastric endoscopic procedures. Gastrointest Endosc 2007;65:497-500. 24. von Delius S, Feussner H, Wilhelm D, et al. Transgastric in vivo histology in the peritoneal cavity using miniprobe-based confocal fluorescence microscopy in an acute porcine model. Endoscopy 2007;39:407-11. 25. Wilhelm D, Meining A, von Delius S, et al. An innovative, safe and sterile sigmoid access (ISSA) for NOTES. Endoscopy 2007;39:401-6. 26. Hu B, Kalloo AN, Chung SSC, et al. Per-oral transgastric endoscopic primary repair of a ventral hernia in a porcine model. Endoscopy 2007;39: 390-3. 27. Onders RP, McGee MF, Marks J, et al. Natural orifice transluminal endoscopic surgery (NOTES) as a diagnostic tool in the intensive care unit. Surg Endosc 2007;21:681-3. 28. American Society for Gastrointestinal Endoscopy/SAGES Working Group, Rattner D, Kalloo A. ASGE/SAGES Working Group on Natural Orifice Translumenal Endoscopic Surgery. October 2005. Surg Endosc 2006;20:329-33.
Volume 68, No. 1 : 2008 GASTROINTESTINAL ENDOSCOPY 65
Flexible transgastric peritoneoscopy and liver biopsy 29. Swain CP. A justification for NOTES: natural orifice translumenal endosurgery. Gastrointest Endosc 2007;66:514-6. 30. Rattner D, Hawes RH. NOTES: gathering momentum. Gastrointest Endosc 2006;63:838-9. 31. Bessler M, Stevens P, Milone L, et al. Transvaginal cholecystectomy, laparoscopically assisted, for gallstones, a human case. SAGES 2007 final program 2007:ET017. 32. WeBSurg’s World Virtual University July 2007. Available at: http://www.websurg.com/notes/experts/index.php. Accessed August 1, 2007. 33. USGI Medical. News June 25 2007. Available at: http://www.usgimedical. com. Accessed August 1, 2007. 34. Marks JM, Ponsky JL, Pearl JP, et al. PEG ‘‘rescue’’: a practical NOTES technique. Surg Endosc 2007;21:816-9. 35. Schweitzer MA, Demaria EJ, Sugerman HA. Laparoscopic Roux-en-Y gastric bypass procedure. Surg Rounds 2000;23:371-80. 36. Schweitzer MA, Lidor A, Magnuson TH. A zero leak rate in 251 consecutive laparoscopic gastric bypass operations using a two-layer gastrojejunostomy technique. J Laparoendosc Adv Surg Tech 2006;16:83-7. 37. Hazey JW, Needleman BJ, Melvin WS, et al. Transgastric instrumentations and bacterial contamination of the peritoneal cavity. SAGES 2007 final program 2007:S044.
66 GASTROINTESTINAL ENDOSCOPY Volume 68, No. 1 : 2008
Steele et al 38. Ponsky JL. Gastroenterologists as surgeons: what they need to know [abstract]. Gastrointest Endosc 2005;61:454. 39. Hochberger J, Lamade W. Transgastric surgery in the abdomen: the dawn of a new era? Gastrointest Endosc 2005;62:293-6. 40. Lamade W, Hochberger J. Transgastric surgery: avoiding pitfalls in the development of a new technique. Gastrointest Endosc 2006;63: 698-700. 41. Fritscher-Ravens A. Transgastric endoscopy: a new fashion, a new excitement! Endoscopy 2007;39:161-7. 42. Reddy DN, Rao GV. Transgastric approach to the peritoneal cavity: are we on the right track? Gastrointest Endosc 2007;65:501-2.
Received August 2, 2007. Accepted September 4, 2007. Current affiliations: Department of Surgery (K.S., M.A.S., J.L.-S.), Division of Gastroenterology (S.V.K.), Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. Reprint requests: Sergey V. Kantsevoy, MD, Division of Gastroenterology, Johns Hopkins Hospital, 1830 East Monument St, Rm 423, Baltimore, MD 21205.
www.giejournal.org