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Ann Surg. 2004 January; 239(1): 22–27. | PMCID: PMC1356188 |
Copyright © 2004 Lippincott Williams & Wilkins, Inc. Double Endoscopic Intraluminal Operation for Upper Digestive Tract Diseases Proposal of a Novel Procedure Hiroyuki Kuwano, MD, PhD, FACS, Erito Mochiki, MD, PhD, Takayuki Asao, MD, PhD, FACS, Hiroyuki Kato, MD, PhD, Tatsuo Shimura, MD, PhD, and Souichi Tsutsumi, MD, PhD From the Department of Surgery I, Faculty of Medicine, Gunma University, Gunma, Japan.
Background and Objective: Endoscopic treatment of digestive tract diseases, such as early esophageal and gastric neoplasia, has become increasingly popular in recent years as an alternative to surgical procedures in the hope of providing an improved quality of life for these patients. However, one of the limitations of a conventional endoscopic mucosal resection, such as an aspiration mucosectomy and a strip biopsy, has been the size of the lesions to be resected. Both an aspiration mucosectomy and strip biopsy are useful variants for removing flat lesions measuring less than 20 mm in maximal diameter. To overcome such limitations, we devised a double endoscopic intraluminal operation (DEILO), which enables us to resect mucosal lesions by using 2 fine endoscopes and monopolar shears. Methods: DEILO was performed on patients with esophageal and gastric lesions measuring up to 40 mm in diameter. This novel technique is characterized by the use of 2 endoscopes (one for lifting the lesion and the other for cutting the lesions) inserted into the esophagus or stomach through an overtube. A mucosal resection is then performed by dissecting the mucosal margin with newly developed monopolar shears, thereby separating the mucosa from the submucosa. Results: A total of 25 lesions in the esophagus (8 lesions) and stomach (17 lesions) were resected by DEILO. The sizes of the esophageal lesions ranged from 8 to 40 mm in diameter (mean, 21.1 mm) whereas gastric lesions ranged from 8 to 30 mm (mean, 13.3 mm) in diameter, and histopathologic examinations revealed the resection margin to be clear and without any tumor. No complications or instances of recurrence were observed in this series. Conclusions: DEILO is considered to be feasible for the mucosal resection of esophageal and gastric lesions measuring more than 10 mm in diameter without submucosal invasion, whereas conventional endoscopic mucosal resection is indicated for such lesions measuring less than 10 mm in size. Endoscopic treatment of esophageal and gastric lesions is a type of minimally invasive surgical treatment and has become increasingly popular in recent years as an alternative to surgical treatment. 1 Laser therapy, which has broken new ground in the endoscopic treatment of gastrointestinal cancer, has been followed and replaced by advances in endoscopic mucosal resection. 1 Takemoto et al described an endoscopic strip biopsy technique for the excision of early gastric cancer. 2 However, this endoscopic technique is limited according to the size of the tumor (less than 20 mm in diameter) and its location (the body and cardia). 3 Recently, an endoscopic mucosal resection (EMR) has been widely accepted for the treatment of early gastric cancer because its minimal invasiveness and the improvement it adds to the patients’ quality of life. 3 EMR has become the standard treatment option for superficial lesions of the esophagus, 4 stomach, and colon. 5 EMR is indicated in esophageal cancer if 1) the infiltration depth is m1 or m2 and 2) the superficial spread is less than half of the circumference. 6 Indications for EMR in gastric cancer include: 1) differentiated adenocarcinoma, 2) mucosal cancer less than 10 mm in diameter in IIb and IIc lesions, and 3) mucosal cancer less than 20 mm in diameter in II a lesion. 7Laparoscopic surgery has recently been widely applied to a variety of gastrointestinal operations. For gastric malignancies, many new laparoscopic devices and procedures have been developed, including a laparoscopic mucosectomy, 8 and a partial or total gastrectomy with a laparoscopic stapler. 9–11 The main advantages of these laparoscopic procedures is that they are less invasive than open gastric operations. 8 However, although an endoscopic mucosal resection is even less invasive than these other laparoscopic procedures, its use is limited by the size and site of the lesion. The maximal size of lesions resected by a laparoscopic mucosectomy is about 30 mm in diameter. However, an endoscopic mucosectomy is limited to tumors measuring less than 20 mm in diameter. Furthermore, laparoscopic intragastric surgery cannot resect the mucosa of the anterior wall of the stomach. 12 To avoid these disadvantages and to also preserve the advantages of EMR and laparoscopic procedures, we herein introduce the novel double endoscopic intraluminal operation (DEILO). The use of 2 fine endoscopes and monopolar shears allows for an easy dissection of the lesion in both the esophageal and gastric lumens. Indications for Endoscopic Treatment Radical endoscopic treatment is indicated for polyps, cancer lesions limited to the mucosa and submucosal tumors, and these lesions cannot be accompanied by either metastatic lymph nodes or distant metastases. EMR in esophageal cancer is indicated for: 1) mucosal cancer less than 20 mm or one third of circumference of the esophagus and 2) esophageal lesions extending as far as the middle layer of the lamina propria mucosae in depth. 13,14 An endoscopic mucosal resection is suitable for gastric superficial depressed type cancers measuring less than 1 cm in diameter as well as superficial elevated type cancers measuring less than 20 mm in diameter. 7,15 In contrast, benign tumors of the esophagus and stomach are indicated for resection when measuring up to 40 mm in diameter in this study. Therefore, in this study a surgeon and gastroenterologist performed a preoperative endoscopic assessment in which the histologic type is confirmed by biopsy specimens and the tumor size was measured by forceps. In cancers, endoscopic ultrasound was used for all cases to determine the depth and size of the tumor or the extent of cancer invasion. In submucosal tumors, endoscopic ultrasound was used to obtain information on their layer of origin and margin. Patients Ten patients with esophageal tumors and 18 patients with gastric tumors were candidates for this procedure. Two patients with esophageal cancer and 1 patient with gastric cancer were ruled out for this procedure by preoperative endoscopic ultrasound studies because of submucosal invasion. At our institution, endoscopic ultrasound studies showed an 83.9% accuracy for the gastric cancer and an 86% accuracy for esophageal cancer. Between June 1999 and September 2001, 8 patients with esophageal lesions and 17 patients with gastric lesions were treated with EMR by DEILO at our department (). | TABLE 1. Clinical Data on 7 Patients With Esophageal Tumors |
| TABLE 2. Clinical Data on 15 Patients With Gastric Tumors |
An EMR was performed out using 2 gastrointestinal endoscopes. All subjects were observed endoscopically at 2 weeks and 1, 3, 6 and 12 months after treatment. An endoscopic biopsy was also performed semiannually thereafter to check for any recurrence. The aims and methods of the study were fully explained to the subjects, and written informed consent was obtained. In addition, the Faculty of Medicine Ethical Committee of Gunma University approved this study. DEILO Technique Before endoscopy was performed, patients were asked about any relevant medical illnesses, previous endoscopic procedures, previous abdominal surgery, and current medications. All patients begin fasting after midnight the evening before DEILO. Medication was given before DEILO to anesthetize the posterior pharynx (Xylocaine Viscous, 200 mg/body, AstraZeneca, London, UK). Sedation is sometimes necessary during endoscopic procedures, especially when such procedures are expected to last longer than 30 minutes. Compared with diagnostic endoscopy, DEILO is more painful because 2 endoscopes are used. Patients receiving only conscious sedation with diazepam (10 mg/body, Takeda Chemical Industries, LTD., Osaka, Japan) and pentazocine hydrochloride (15 mg/body, Sakyo Co., LTD., Tokyo, Japan) may therefore respond to painful stimuli during the endoscopic procedure. We used 2 gastrointestinal endoscopes for EMR. The first endoscope was XQ240 (Olympus, Tokyo, Japan), which measured 9 mm in the outer diameter. The second endoscope was N230 (Olympus), which measured 6.6 mm in the outer diameter. In cases in which the tumor could not be seen directly from the front of the lesions, a side-viewing endoscope (PJF-7.5, Olympus) was used to see the tumor directly. The first gastrointestinal endoscope (XQ240) with a short (20 cm) overtube was premounted over the endoscope to stent the crico pharyngeus and then was inserted into the stomach. This over tube (single use; MD-48618, Sumitomo Bakelite Co., LTD., Tokyo, Japan), modified in our laboratory, facilitates multiple insertions and allows for the insertion of a second gastrointestinal endoscope. An over tube should be introduced with guidance over an endoscope. Liberal lubrication of the overtube and endoscope is critical before insertion. The superficial extent of mucosal cancer and benign tumor is often difficult to recognize accurately in routine endoscopic observations. For squamous cell carcinoma of the esophagus, an iodine solution is the most effective dye and shows the lesion clearly as an uncolored area. In gastric cancer and adenoma, spraying indigo carmine solution emphasizes the surface characteristics. After spraying dye solution onto the mucosa, the mucosal surface that surrounds the margin of the lesion is carefully marked by the tip of the snare wire with electrocautery by the first gastrointestinal endoscope. Markings are positioned 2 mm apart from the margin of the lesion. 5,16 In submucosal tumors, endoscopic ultrasound was used to have the information of their margin. Thereafter, needle forceps are inserted into the submucosa under the lesion. Five to 10 mL of epinephrine saline solution diluted 10,000 times (0.1% epinephrine solution, 1.0 mL, plus normal saline 100 mL) is then injected into the submucosa through the needle forceps to prevent bleeding until the target lesion is elevated. By means of the submucosal injection of physiological saline and formation of an artificial elevation, EMR allows for a wide resection of a lesion along with the surrounding normal mucosa. The second endoscope is inserted into either the esophagus or the stomach and the edge of the lesion is slightly elevated using a biopsy forceps . The mucosal resection is started by dissecting the mucosal margin with newly developed monopolar shears , thereby separating the mucosa from the submucosa . The newly developed monopolar shears are able to cut any mucosa while simultaneously coagulating the bleeding vessels. They can grasp the mucosa but cannot cut it without an electrical current source. The important techniques that are required for DEILO include grasping and pulling up the tissue by the forceps and then excising the mucosa using electrocautery and monopolar shears. The monopolar shears are able to dissect the loose connective tissue of the submucosa while leaving the remaining muscle layer intact. The resected specimen is removed by using grasping forceps through the overtube without any need to use a receiving bag. The resected specimen was stretched and fixed on a rubber plate using fine needles and then was bathed in 10% formalin solution. The respectability of DEILO specimens was carefully evaluated histopathologically in slices made at 2-mm intervals according to the Japanese Classification of Gastric Carcinoma. 16,17All procedures were done while carefully monitoring patient’s vitals and oxygenation. After the procedure, the clinical status of patients was observed in first operative hours and all patients had chest x-rays to identify any complications, such as pharyngeal, esophageal, or gastric perforation, and then they were returned to their hospital room. Antibiotics were administered intravenously for the first 2 days. The following day, the patient received a soft meal. The second day after treatment, the patient was allowed to resume a normal diet. In this series, a total of 25 lesions in the esophagus and stomach were resected by using our EMR technique. The mean hospital stay was 3 days. The duration of the EMR ranged from 30 to 90 minutes (mean, 48 minutes), as shown in . For the DEILO operation that took 90 minutes, the tumor size was 40 mm in diameter. None of the patients suffered perforation, and 2 patients experienced minor mucosal bleeding during the procedure. All bleeding was controlled by spraying a thrombin solution onto the bleeding site. Up to now, no treatment-related complications or deaths have been observed. Of the 25 lesions resected, 8 were esophageal and 17 were gastric. Four of 8 esophageal lesions were benign, and 9 of 17 of gastric lesions were benign . The remaining lesions consisted of 8 cancers, 2 squamous papillomas, 1 dysplasia, and 1 gastrointestinal stromal tumor. Endoscopic mucosal resections of the esophagus have been performed for 8 lesions in 8 patients . The esophageal tumors were located in the middle intrathoracic esophagus in 5 patients and in the lower intrathoracic esophagus in 3 patients. The size of the lesions ranged from 8 to 40 mm in diameter (mean, 21.1 mm). Eight lesions of esophagus (8/8) were completely resected and all lesions were resected en bloc. Regarding esophageal cancer, histopathological examinations showed that cancer had infiltrated to the middle layer of the lamina propria mucosae in 1 case (see , patient 8). If the esophageal cancer invades the lamina muscularis mucosa according to histopathological evaluations of the resected specimen, then additional laparoscopic or conventional open surgery with lymph node dissection or irradiation is considered to be necessary. Regarding the clinical outcome, no esophageal lesions have so far developed any local recurrence at present during a 1- to 3-year follow-up period. Endoscopic mucosal resections of the stomach were performed for 17 lesions in 17 patients . A gastric tumor was located in the upper portion of the stomach in 1 patient, in the middle portion of the stomach in 6 patients, and in the lower portion of the stomach in 10 patients. Two lesions on the lesser curvature in the upper portion and the middle portion of the stomach could not be resected en bloc (, patients 5 and 8). If an additional resection is necessary to completely remove any residual lesions, then all of the procedures, including saline injection, are repeated step by step. The remaining 15 lesions (88.2%) were all completely resected en bloc. The size of the lesions ranged from 8 to 30 mm in diameter (mean, 13.3 mm). Histopathological examinations showed all cancers (7 cases) to have intramucosal invasion and they were thus all resected with a clear lateral margin. Regarding the clinical outcome, no gastric lesions developed local recurrence during a 1- to 3-year follow-up period. Recent progress in the detection of early esophageal and gastric cancer have made an endoscopic mucosal resection possible for the treatment of these cancers instead of only a conventional esophagectomy or gastrectomy. Noninvasive treatments, such as a strip biopsy or EMR using a gastrofiberscope, and improved modalities, such as an aspiration mucosectomy, 5 have been increasingly applied to early esophageal or gastric cancers. 1,2 Although EMR is minimally invasive, its application is limited by the site and size of the lesion. 3,4 In the past study, an incomplete resection usually occurred when lesions had a diameter exceeding 10 mm and were situated in the body and cardia. 3 Takekoshi et al reported that the entire margin was difficult to visualize using a front-view endoscope, especially in lesions on the anterior wall or posterior wall of the gastric angle or body. 7 Our new technique, DEILO, enables us to access lesions on the anterior wall and posterior wall of the gastric body using a side-viewing endoscope. Moreover, the advantages of DEILO are: 1) the mucosal layer is easily grasped and lifted up using the grasping forceps and 2) the newly developed monopolar shears are able to dissect the tissue without bleeding. The DEILO technique is a type of intraluminal surgery of the esophagus and stomach in which 2 endoscopes are inserted per orally. Our study is the first report to describe this type of technique, using 2 fine endoscopes. DEILO can be performed not only by surgeons but also by gastroenterologists. However, for a successful endoscopic mucosal resection, DEILO requires more skill than any other technique. The average diameter of specimens for an endoscopic mucosal resection is 15.8 mm, and the one-piece resection rate was 92% in our study. Ohkuwa et al reported one-piece resection rates of 82% for lesions measuring 10 mm or less, 75% for those between 11 and 20 mm, and 14% for those of over 20 mm. 18 Therefore, the size of the lesion affected the cure rate with EMR. Compared with conventional EMR, DEILO has some significant benefits, particularly regarding a one-piece resection of esophageal and gastric lesions measuring between 8 and 40 mm in size. Moreover, histologic evaluations are easier after the introduction of this technique because of a one-piece resection. If the gastric cancer invades the submucosa based on a histopathological evaluation of the resected specimen, then additional laparoscopic surgery with lymph node dissection is considered to be necessary. If an additional resection is necessary to remove the residual lesion due to a positive lateral margin, then EMR or laser therapy should be performed. 16A piecemeal endoscopic mucosal resection often results in an incomplete resection in which a surgical margin of the specimen is histopathologically unclear. As a result, laparoscopic surgery is thus considered to be better for the treatment of mucosal gastric cancer than EMR, if the size of the lesion is larger than 10 mm or the site of the lesion is near the cardia where EMR is technically difficult to perform. 9 To reduce the operative invasiveness of the laparoscopic gastrectomy, both a laparoscopic wedge resection of the stomach using a lesion-lifting method 19 and laparoscopic intraluminal (intragastric) surgery 12 have recently been introduced. To overcome the limitations of EMR (especially regarding the size of the lesion) and to maintain the noninvasive advantages of this procedure, we developed the double endoscopic intraluminal operation (DEILO) for the resection of mucosal lesions in the upper digestive tract, such as in the esophagus and the stomach. Although it is still difficult to treat lesions located near the gastric cardia, we could nevertheless successfully perform this procedure not only for small lesions but also for large mucosal lesions. In most endoscopes, it is possible to turn the tip of the bending section more than 100 degrees to allow for a sufficient inspection of such surfaces as the cardia. However our technique is difficult to treat lesions located near the gastric cardia because the 2 endoscopes tended to interfere with each other when turning the tip of the bending section. We think that DEILO can thus be further improved with continuing advances in instrumentation. Perforation and bleeding are major complications of EMR. However, no perforation or major bleeding occurred in any of our cases. For the prevention of perforations, sufficient saline should be injected into the submucosal layer to raise the mucosa containing the lesion. Moreover, in our technique, using monopolar shears also prevents perforation, because it is able to dissect the loose tissue of the submucosa while leaving the remaining muscle layer intact. The mean period of hospitalization for patients treated by DEILO was 3 days. It may be possible to reduce this period, which seems to be associated with the Japanese health insurance system. In our experience, DEILO can also be performed on an outpatient basis. Our follow-up schedule has 5 examinations within a year after EMR. Follow-up endoscopies at 2 weeks, 1 month, and 3 months after treatment are used to monitor the healing process of the artificially induced ulcer after DEILO. There is a small possibility that persistent stenosis of the esophageal or gastric lumen might occur after an artificial ulcer heals, and such stenosis can develop after a near-total circumferential resection in the esophagus or prepylorus in the stomach is performed. 20Consequently, this technique was found to be effective for the treatment of esophageal and gastric mucosal lesions, except for those located near the gastric cardia. DEILO is considered to be feasible for a mucosal resection of esophageal and gastric lesions measuring more than 10 mm in diameter without submucosal invasion, whereas conventional EMR is indicated for such lesions measuring less than 10 mm, in which the cutting line can be easily controlled. 1. Takeshita K, Tani M, Inoue H, et al. Endoscopic treatment of early oesophageal or gastric cancer. Gut. 1997;40:123–127. [PMC free article] [PubMed] 2. Takemoto T, Tada M, Yanai H, et al. 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