Abstract
Background/Aim: Laparoscopy and endoscopy cooperative surgery (LECS) is an excellent surgical procedure that utilizes the advantages of both methods. This study was designed in our hospital to evaluate the clinical usefulness of LECS for the removal of gastric submucosal tumors after its standardization. Patients and Methods: Between 2007 and 2015, 62 consecutive patients underwent surgical resection for gastric submucosal tumors. LECS has been standardized since 2010. Results: (i) There were no significant differences in background factors between patients (such as sex, age, body mass index (BMI), tumor size and postoperative complications), before or after the standardization of LECS. However, after the standardization of LECS, patients had a lower incidence of gastrectomy and wedge resection (WR) (p<0.001), a smaller amount of blood loss (p=0.001) and a shorter hospital stay after surgery (p<0.001) than those before standardization. (ii) LECS was associated with a significantly shorter maximum surgical margin of resected tumors (p=0.020, LECS vs. WR=10.0 vs. 15.0 mm) compared to WR. Patients with upper-third tumors were more frequently treated by LECS than by WR (p=0.014; LECS vs. WR=76 % vs. 27 %). Conclusion: Standardization of LECS contributes to reduction of unnecessary gastrectomy for gastric submucosal tumors. In particular, LECS may have merit in the removal of upper-third tumors by avoiding wedge resection, which carries the risk of excessive resection and deformity of the stomach.
Recent advances in screening examinations, such as upper gastrointestinal endoscopy, and other modalities, have resulted in gastric submucosal tumors being frequently found (1, 2). Especially in highly malignant gastric submucosal tumors, such as gastrointestinal stromal tumors (GIST), partial resection using laparoscopic surgery and open surgery have common indications according to the Japanese (3, 4) and National Comprehensive Cancer Network (NCCN) guidelines.
Until recently, wedge resection (WR) (5, 6) or alternative gastrectomy have been mainly performed, despite accurate pre- and intraoperative information on tumor location in the stomach and tumor type (intra- or extragastric growth type). WR may require a relatively large resection of the gastric wall causing subsequent deformity and be a potential risk for reduced oral intake, whereas alternative gastrectomy for tumors near the esophago-gastric junction or pylorus, performed to avoid the definite risk of subsequent deformity due to WR (7-9), has a high probability of causing post-gastrectomy syndromes and nutritional disorders (10-13).
Recently, Hiki et al. developed laparoscopy and endoscopy cooperative surgery (LECS) (14), a promising procedure to resolve the above-mentioned problems, for gastric submucosal tumors. LECS is an excellent surgical procedure that utilizes the advantages of both the laparoscopic and endoscopic approaches. Namely, LECS enables surgeons and endoscopists to intraoperatively select appropriate cutting and suturing lines using both approaches (15-18) and contributes to potentially maintaining gastric motility (19). In our hospital, LECS was introduced and standardized since 2010. In this study, we investigated the clinical usefulness of LECS for gastric submucosal tumor by comparing clinical data before and after its standardization in our hospital. The results of our study may provide evidence that standardization of LECS contributes to treatment of gastric submucosal tumors.
Patients and Methods
Patients and surgical procedures. Between 2007 and 2015, 62 consecutive patients with gastric submucosal tumors underwent curative surgical resection at the Department of Digestive Surgery, Kyoto Prefectural University of Medicine. In nearly all cases, surgical indications were determined according to endoscopy, malignant features of endoscopic ultrasonography (EUS), EUS-guided fine needle aspiration (EUS-FNA) biopsy, computed tomography (CT), symptoms, growth of lesion and laboratory tests. Partial resection or gastrectomy and open or laparoscopic surgery were decided according to the Japanese guidelines for the treatment of gastric cancer (3, 4). LECS is normally indicated for gastric submucosal tumors with a tumor size <50 mm in diameter as a preoperative diagnosis, regardless of tumor location. Moreover, excluding the typical extragastric growth type, LECS was performed in almost all tumors after standardization in our hospital, whether or not there was an unclear resection margin on the peritoneal side. However, LECS was avoided in lesions with ulceration to prevent the risk of intraperitoneal dissemination. All patients provided their written, informed consent for the proposed procedure; a traditional gastrectomy or wedge resection was offered as an option before treatment.
Surgical procedure of LECS. The patients were placed in the supine position. The laparoscopic surgeon stood on either side of the patient, according to tumor location, and the endoscopist stood on the left. The laparoscopic surgeon placed the operative ports in the standard position for upper gastrointestinal procedures. First, the tumor location was endoscopically-confirmed and a submucosal dissection followed, using an insulated tip electrosurgical knife (IT Knife; Olympus, Tokyo, Japan) to determine an appropriate resection line (Figure 1A). To minimize the resection of the stomach wall, almost all types of submucosal tumors were followed by intraoperative endoscopic examination and/or submucosal dissection, excluding a typical extragastric growth type.
Next, prior to tumor resection, the laparoscopic surgeon selected the best anastomotic axis to avoid deformity of the stomach (Figure 1B) and made marking sutures at the start and end points of a possible anastomosis line (Figure 1C). Then, the endoscopist made a perforation of the gastric wall at the start point of the dissection line using a standard needle knife and, afterwards, the seromuscular layer was laparoscopically dissected (Figure 1D). The specimen was protected in a plastic bag and retrieved through an umbilical port hole. Finally, the incision line was lifted (Figure 1E) and closed using a laparoscopic stapling device (Figure 1F). For tumors located near the esophagogastric junction or pyloric ring, the gastric wall was often closed by laparoscopic hand-sewing because a stapling device in these areas may potentially cause anastomotic leakage, deformity of the stomach or stenosis.
Treatments following surgical resection. All patients were followed at the outpatient clinic where abdominal ultrasounds and CTs were performed every 6-12 months after surgery. Based on the treatment guideline (3, 4), patients with high-risk or clinically malignant tumors were treated with antitumor drugs or intensive follow-up examinations using CT every 4-6 months after surgery. There were recurrences in two patients. One patient with GIST had a peritoneal dissemination, while one patient with liposarcoma had a peritoneal dissemination. There was no recurrent patient undergoing LECS.
Evaluation of clinical impact of LECS after standardization in our hospital. To clarify the clinical merits of standardization of LECS for gastric submucosal tumors, we initially compared the clinicopathological and surgical data between patients before and after standardization of LECS in our hospital (Table I). We also compared the clinicopathological and surgical data of LECS and wedge resection (WR) to evaluate and compare their usefulness in a partial resection (Table II).
Statistical analysis. The Chi-square and Fisher's exact probability tests were performed for the categorical variables, while the Student's t-test and Mann-Whitney U-test for unpaired data of continuous variables were performed to compare clinicopathological characteristics between the two groups. A p-value of less than 0.05 was considered significant.
Results
Clinicopathological characteristics of patients with gastric submucosal tumors. The clinical characteristics of 62 patients undergoing surgical resection of gastric submucosal tumors were as follows. The study group consisted of 32 male and 30 female patients with a median age of 65 years (range=30-88 years). The median tumor size was 32.0 mm (range=8-80 mm). No patient had any anastomotic complications or reflux esophagitis.
Pathologically, the 62 patients with gastric submucosal tumors were diagnosed as follows: 54 patients with GIST, 2 patients with schwannoma, 2 patients with carcinoma, one patient with carcinoid tumor, one patient with leiomyosarcoma, one patient with liposarcoma and one patient with lipoma. Thirty-three (53%) patients underwent LECS, 15 (24%) patients underwent WR and 14 (23%) patients underwent gastrectomy (8 of distal gastrectomy, 5 of proximal gastrectomy and 1 of total gastrectomy). All enrolled patients underwent macroscopic and pathologically curative resection (R0).
Comparison of clinicopathological features between patients before and after standardization of LECS. LECS has been standardized since 2010 in our hospital. Of the 62 total patients, the number of patients before and after standardization of LECS were 19 and 43, respectively. Table I shows that, between the two groups, there were no significant differences in background factors, such as sex, age, body mass index (BMI), tumor size and postoperative complications. Patients after standardization of LECS had a lower incidence of both gastrectomy and WR (p<0.001). Specifically, the incidence of gastrectomy before standardization of LECS was reduced from 37% to 16% after standardization (p=0.074). The standardization of LECS contributed significantly to a shorter hospital stay after surgery (p<0.001) and a higher incidence of referred and treated patients with upper-third tumors (p<0.001) than before standardization.
Surgical procedure of LECS in a typical case concerning an elderly female patient who had a 35x35 mm GIST located at the anterior and lesser curvature of the upper-stomach near the esophagogastric junction. Details are given in the Patients and Methods section under the subheading “Surgical procedure of LECS”.
Comparison of clinical features between patients undergoing LECS and WR. Table II shows the comparison of clinical features between LECS (n=33) and WR (n=15) in 48 patients undergoing partial resection. There were no significant differences in clinical factors, such as sex, age, BMI, tumor size and postoperative complications. Patients with upper-third tumors were more frequently treated by LECS than WR (p=0.014; LECS vs. WR=76 % vs. 27 %). Also, LECS was associated with a significantly shorter maximum surgical margin of resected tumors (p=0.007, LECS vs. WR=10.0 vs. 15.0 mm), indicating the suitability of LECS for upper-third gastric submucosal tumors by preventing the excessive resection and deformity of the stomach.
Comparison of clinicopathological features between patients before and after standardization of LECS.
Discussion
Unnecessary gastrectomy for gastric submucosal tumors may cause postgastrectomy syndromes and nutritional disorders (10-13) that result in a reduced quality of life (QoL). Even with WR, a relatively large resection of the gastric wall may cause subsequent deformity, which is a potential risk for reduced oral intake (5, 6). Previously, WR or alternative gastrectomy have been routinely performed for gastric submucosal tumors. In this study, we clearly demonstrated that the standardization of LECS in our hospital significantly reduced the incidence of gastrectomy and WR for gastric submucosal tumors. Moreover, LECS was safely performed without any postoperative complications, thus rendering this approach particularly beneficial in preventing the risk of excessive resection of the stomach in upper-third tumors.
This study demonstrates some benefits of LECS standardization, including a better indication for upper or lower tumors, a lower amount of blood loss, a lower incidence of postoperative complications and a shorter hospital stay. However, LECS may require a significantly longer operation time (Table I). In cooperative surgery, a long operation time may be an inevitable disadvantage; therefore, based on our experience, we can suggest ways to reduce LECS operation time and complications. Specifically, we made marking sutures at the start and end points of a possible anastomosis line to secure the best anastomotic axis prior to tumor resection and avoid deformity of the stomach. Since the size of the stomach hole after tumor resection could be larger, it is sometimes difficult to select the anastomotic axis and requires time to decide on the best anastomotic line. Moreover, these marking sutures were helpful in lifting the stomach, which prevented spilling of stomach fluids that causes the potential risk of peritoneal dissemination. Also, a laparoscopic surgeon can move the stomach to provide a better axis for the endoscopist to easily dissect during the endoscopic approach. In addition, we have herein shown that, in order to minimize the resection of the stomach wall, almost all types of submucosal tumor were followed by intraoperative endoscopic examination and/or submucosal dissection, excluding a typical extragastric growth type. To treat tumors located near the esophagogastric junction, the gastric wall was often closed using a hand-sewing technique since, using a stapling device in these areas, could potentially cause anastomotic failure due to the high tension to stapling suture lines and deformity due to the stiffness of the stapler anastomosis. Furthermore, we performed an anti-reflux surgery, in addition to LECS, for tumors located extremely close to or on the esophagogastric junction and fornix.
Comparison of clinical features between patients undergoing LECS and WR.
An unexpected benefit of LECS standardization, shown in Table I, is that referred patients with upper-third tumors near the esophagogastric junction tended to increase after standardization of LECS (p=0.074). Since February 2014, the LECS procedure for gastric tumor has been on the national insurance list in Japan and its use is rapidly increasing in Japanese institutions (20, 21). In our institute, referred patients planned for LECS are indeed markedly increasing in numbers after the standardization of the procedure. The reason is that general practitioners and gastrointestinal doctors already know the merits of LECS and prefer this approach as it helps maintaining a high QoL for their patients.
LECS is a new and promising surgical procedure that utilizes the advantages of both laparoscopic and endoscopic approaches. Nonetheless, there are several limitations to be resolved. First, classical LECS is not suitable for gastric submucosal tumors that are ulcerated and exposed because of the risk of tumor seeding into the peritoneum during the procedure. This is also a challenge in the application of LECS for cancerous lesions. To resolve this problem, various cooperative techniques have already been reported (22-25). These promising techniques are under evaluation and we hope to report on their usefulness in the near future. Second, although LECS is applicable for other gastrointestinal malignancies, such as in the duodenum, small intestine and colon (26, 27), the national insurance for the LECS procedure in Japan is currently restricted to the stomach and does not cover tumors of other parts of the gastrointestinal tract. Using LECS, the technical difficulties could be shared by laparoscopic surgeons and endoscopists for many types of tumors. It is also important to note that clinical difficulties and adverse events encountered by the endoscopic surgeon may be safely recovered by the laparoscopic surgeon using LECS (26-28).
The main limitation of the present study is that it is a relatively small, retrospective cohort study from a single institute. Therefore, a larger cohort or observational study is needed to validate the favorable effects of LECS on gastrointestinal tumors, as well as gastric submucosal tumors. In conclusion, the standardization of LECS contributes to increasing referred patients, as well as reducing unnecessary gastrectomy for gastric submucosal tumors. LECS may be of particular value in upper-third tumors by avoiding WR, which carries the risk of excessive resection and deformity of the stomach.
- Received March 31, 2016.
- Revision received May 8, 2016.
- Accepted May 9, 2016.
- Copyright© 2016 International Institute of Anticancer Research (Dr. John G. Delinassios), All rights reserved
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