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Asian J Endosc Surg ISSN 1758-5902

O R I G I N A L A RT I C L E

Clinical outcomes of laparoscopic partial gastrectomy for gastric submucosal tumors Masashi Hirota,1 Kiyokazu Nakajima,1 Yasuhiro Miyazaki,1 Tsuyoshi Takahashi,1 Yukinori Kurokawa,1 Makoto Yamasaki,1 Hiroshi Miyata,1 Shuji Takiguchi,1 Toshirou Nishida,2 Masaki Mori1 & Yuichiro Doki1 1 Department of Surgery, Osaka University Graduate School of Medicine, Osaka, Japan 2 National Cancer Center Hospital East, Chiba, Japan

Keywords Gastric remnant function; laparoscopic surgery; partial gastrectomy Correspondence Kiyokazu Nakajima, Department of Surgery, Osaka University Graduate School of Medicine, 2-2, E-2, Yamadaoka, Suita, Osaka 565-0871, Japan. Tel: +81 6 6879 3251 Fax: +81 6 6879 3259 Email: [email protected] Received 12 July 2014; accepted 31 August 2014 DOI:10.1111/ases.12145

Abstract Introduction: Laparoscopic partial gastrectomy has become a common procedure for gastric submucosal tumors because of its accepted feasibility, safety, and oncologic outcomes. However, long-term postoperative outcomes have not been determined, especially based on the location of submucosal tumors. Methods: We reviewed 52 consecutive gastric submucosal tumor patients who underwent laparoscopic partial gastrectomy between 1999 and 2009. They were divided into a lesser curvature group (LC group, n = 23) and a greater curvature group (GC group, n = 26) according to tumor location. We compared the following postoperative data about gastric function between the two groups: (i) body weight change during the first postoperative year; (ii) gastrointestinal symptoms (e.g. abdominal pain/discomfort, bloating, heartburn, and dyspepsia); (iii) the amount of food residue at endoscopy; and (iv) the need for medications such as histamine H2-receptor antagonists, proton pump inhibitors, and prokinetic drugs. Results: Only a few patients – one in the LC group and two in the GC group – showed body weight loss (over 10%). Compared to the GC group (n = 0 in all three categories), the LC group showed significantly higher frequency of prolonged postoperative abdominal symptoms (n = 4, P = 0.042), food residue at endoscopic follow-up (n = 4, P = 0.036), and postoperative medication use (n = 5, P = 0.016). Conclusion: Patients who received laparoscopic partial gastrectomy did not have severe body weight loss, which suggests dysfunction of the gastric remnant. However, patients in the LC group should receive special attention, as they have a higher risk of developing postoperative gastrointestinal symptoms.

Introduction Laparoscopic partial gastrectomy (i.e. wedge resection of the stomach) has rapidly gained clinical acceptance as the definitive treatment for gastric submucosal tumors (SMT) such as gastrointestinal stromal tumors (GIST), leiomyomas, and schwannomas. Its technical feasibility, safety, and oncologic application have been identified in some of the surgical literature (1–3), and updated practice guidelines are obliged to describe the use of laparoscopy for GIST smaller than 5 cm in diameter (4).

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In contrast to the recent accumulation of surgical and oncologic evidence, it remains unclear whether laparoscopic partial gastrectomy is appropriate for gastric SMT in terms of functional outcome. This procedure theoretically can cause deformity, dysmotility, axis deviation, and stricture of the gastric remnant depending on the tumor location. However, to the best of our knowledge, few reports have investigated postoperative functional outcomes after laparoscopic partial gastrectomy. The objective of the present study was to evaluate the function of the gastric remnant following laparoscopic partial

Asian J Endosc Surg 8 (2015) 24–28 © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd.

Functional impact of partial gastrectomy

M Hirota et al.

gastrectomy for gastric SMT with regard to tumor location.

Materials and Methods This study was a single-center, retrospective study that was approved by the ethics committee of the Osaka University Graduate School of Medicine. We performed a retrospective analysis of 52 consecutive patients with gastric SMT who underwent laparoscopic R0 resection. We got informed consent from all patients. No patient had a history of stomach surgery. The study sample included all patients with gastric SMT scheduled for laparoscopic partial gastrectomy, without lymph node dissection, between January 1999 and December 2009. We prepared no exclusion criteria related to tumor size or location. Patients who underwent preoperative and/or postoperative chemotherapy were excluded from this study because GI symptoms caused by chemotherapy could introduce bias in evaluating postoperative GI symptoms. The same surgical team performed all surgeries. We divided the patients into a lesser curvature group (LC group, n = 23) and a greater curvature group (GC group, n = 26) according to tumor location. During this categorization, two patients with a tumor in the anterior wall and one patient with a tumor in the posterior wall were excluded. We obtained patients’ background data, which included age, gender, body weight at surgery, size and location of tumor, histopathologic diagnosis, operative time, blood loss, and complications, from a prospectively compiled database,. Patients attended follow-up postoperative evaluations every 4−6 months at an outpatient clinic and underwent abdominal CT and endoscopy. Oncologic follow-up data, such as tumor recurrence or metastasis and functional outcome, were also registered. We obtained data for the following functional parameters: (i) body weight at every outpatient visit during the first postoperative year; (ii) GI symptoms (e.g. abdominal pain/discomfort, bloating, heartburn, and dyspepsia) at endoscopy every 6 or 12 months postoperatively; (iii) the amount of food residue at endoscopy every 6 or 12 months postoperatively; and (iv) the need for postoperative medication, including histamine H2-receptor antagonists, proton pump inhibitors, and prokinetic drugs. Through 2005, postoperative endoscopy was performed at 12 months, and beginning in 2006, it was performed at 6 months postoperatively. Patients with prolonged GI symptoms (i.e. for longer than 1 month) or patients with objective abnormality in esophagogastroduodenoscopy findings received medications such as histamine H2-receptor antagonists, proton pump inhibi-

Figure 1 Gastric resection using a linear stapling device in straight laparoscopy.

tors, and prokinetic drugs, while the other patients did not require medication. With regard to the preparation for endoscopy, patients consumed a low-residue diet the evening before endoscopy and fasted for more than 12 hours before the procedure. We evaluated the amount of food residue at endoscopy according to the RGB (residue, gastritis, bile) classification scheme (5). This classification proposed by Kubo et al. is used for the endoscopic evaluation of the remnant stomach after gastrectomy and is straightforward and practical. In the RGB classification, the amount of residual food is classified into five groups, the degree and extent of gastritis is classified into five groups, and bile is classified into two grades. Our laparoscopic partial gastrectomy technique has been described elsewhere (2). Briefly, with a three- or four-port technique, the stomach was mobilized laparoscopically using monopolar and/or ultrasonic coagulating shears. Any branches of the vagus nerve were positively identified and preserved during dissection. The portion of the stomach that included the lesion was then resected with a laparoscopic linear stapling device with gastrointestinal reloads (Figure 1). When the lesion was located in the lesser curvature and/or adjacent to the esophagogastric junction or the pyloric ring, laparoscopy-assisted surgery with scheduled minilaparotomy was performed. We did not use a stapling device but instead adopted a hand-sewing technique when deformity, narrowing, or axis deviation of the gastric remnant was anticipated (Figure 2). All surgical resections were non-anatomic wedge resections with 5−10-mm margins. Before stapling or resection, the gastric lumen was calibrated with intraoperative CO2feeding gastroscopy. The surgical technique used was selected by the surgeon preoperatively, with consideration for the size, location, and growth pattern of the tumor.

Asian J Endosc Surg 8 (2015) 24–28 © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd.

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Table 1 Patient backgrounds, operative characteristics, and perioperative outcomes

Figure 2 Gastric resection using the hand-sewing technique in laparoscopy-assisted surgery.

A statistical software package (JMP 10, SAS Institute, Cary, USA) was used to compare differences between data. A P-value < 0.05 was considered statistically significant. Mean and standard deviation values are reported unless otherwise indicated.

Age (years) Male/female (n) Tumor size† (cm) Tumor longitudinal location‡ (n) Upper Middle Lower Histological diagnosis (n) GIST Schwannoma Other§ Surgical technique (n) Straight laparoscopy Laparoscopy-assisted surgery Operative time (min) Estimated blood loss (mL) Postoperative length of stay (days) Postoperative complications (n)

Lesser curvature (n = 23)

Greater curvature (n = 26)

P-value

56.5 ± 14.0 9/14 3.8 ± 1.9

60.0 ± 10.1 5/21 4.0 ± 1.5

NS NS NS

9 12 2

11 11 4

NS

18 2 3

18 5 3

NS

12 11

22 4

0.028

134 ± 37 54 ± 52 11.8 ± 6.7

126 ± 61 39 ± 52 9.4 ± 2.6

NS NS NS



2††

NS



Results Patient backgrounds are shown in Table 1. There were no significant differences between the two groups with regard to background. All operations used the laparoscopic approach, but the number of patients who underwent laparoscopy-assisted surgery was significantly larger in the LC group than in the GC group (P = 0.028). The operative time, estimated blood loss, and length of hospital stay after surgery were comparable between the groups. For both groups, the postoperative course was generally uneventful, with the exception of three patients who had a tumor in the GC group; one developed a blood stream infection and two had a superficial surgical-site infection. By the 12-month follow-up, three patients (one in the LC group and two in the GC group) had lost more than 10% of their primary weight (Table 2). There was no significant difference in the mean ratio of body weight loss between the two groups (2.2 ± 5.5% in the LC group and 1.8 ± 6.0% in the GC group). In contrast, prolonged gastrointestinal symptoms were observed in four patients in the LC group (bloating sensation in two and epigastric discomfort in two), all of whom had no GI symptoms preoperatively. In the LC group, four patients showed food residue at endoscopic follow-up; two of them were classified as grade 1, one as grade 2, and one as grade 3

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Size obtained at surgery (resected specimen). ‡According to the Japanese Classification of Gastric Carcinoma, 14th edition. §Includes lipoma, ectopic pancreas, and leiomyoma. ¶Blood stream infection. ††Superficial surgical-site infection. GIST, gastrointestinal stromal tumor; NS, not significant.

Table 2 Evaluation of gastric remnant function

Body weight loss > 10% (yes/no) (n) Body weight decrease Prolonged GI symptom (yes/no) (n) Bloating sensation Epigastric discomfort Food residue at endoscopic follow-up (yes/no) (n) Postoperative medication (yes/no) (n) Proton pump inhibitors Mosapride

Lesser curvature (n = 23)

Greater curvature (n = 26)

P-value

1/22

2/24

NS

2.2 ± 5.5% 4/19

1.8 ± 6.0% 0/26

NS 0.042

2 (8.7%) 2 (8.7%) 4/16

0 (0%) 0 (0%) 0/26

0.036

5/18

0/26

0.018

3 4

0 0

NS, not significant.

according to the RGB classification. The ratio of food residue was significantly higher in the LC group than in the GC group (21% vs 0%, P = 0.036). Moreover, five patients required postoperative medication in the LC

Asian J Endosc Surg 8 (2015) 24–28 © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd.

Functional impact of partial gastrectomy

M Hirota et al.

group; two required prokinetics, one required proton pump inhibitors, and two required the both drugs. The ratio of the patients who required medication was significantly higher in the LC group than in the GC group (28% vs 0%, P = 0.018). The majority of patients (n = 36, 73%) had GIST, and the average tumor size was 3.9 ± 1.7 cm. Positive staining for c-kit or platelet-derived growth factor receptor on immunochemistry analysis was confirmed in all GIST patients. Risk stratification results according to Fletcher’s classification were similar between the LC and GC groups (very low/low/intermediate/high: 1/13/4/0 vs 0/14/4/0, P = 0.5954) (6). All 49 patients were followed up in our outpatient clinic. Recurrence or metastasis was not observed in the series within the mean follow-up period of 58.1 ± 23.6 months.

Discussion The principle of surgery for SMT/GIST that originates in the stomach is similar to that for lesions of other origins: complete resection of tumors with any involved structures. Because wide resections and extensive lymphadenectomies are usually not required, laparoscopic partial gastrectomy is considered reasonable for gastric SMT and has been increasingly reported in the surgical literature (1–3). However, there is an apparent paucity of data in the literature regarding functional outcomes after laparoscopic SMT surgery. Our present work confirmed that laparoscopic partial gastrectomy for gastric SMT is clinically acceptable in terms of the overall postoperative functional outcome of the gastric remnant, early operative results, and longterm oncologic outcomes. Only a few patients overall showed significant body weight loss. These rates are clinically acceptable when compared to those following distal or total gastrectomy, which have been reported to be 9.8% and 13.6%, respectively (7). However, our data also suggest that patients in the LC group had a significantly higher frequency of prolonged postoperative GI symptoms, presence of food residue at endoscopic follow-up, and postoperative medication use than patients in the GC group. Because the functional parameters in this study were not sufficiently objective, we used RGB classification when evaluating the amount of food residue to ensure objectivity. Although it was reported that the interrater agreement was over 93.0% (5), the RGB classification has a subjective aspect in classifying food residue and gastritis. In future studies, more objective measurements (e.g. gastric emptying) will be required for better objectivity. In our study, the time points of the postoperative

endoscopy and medication use were not standardized. These are the limitations of our endoscopic evaluation. There were significantly more patients who underwent laparoscopy-assisted surgery in the LC group than in the GC group. Because we always perform intraoperative CO2-feeding endoscopy for calibration, it is unlikely that the surgical technique is the reason for the functional outcome differences between the two groups. In addition, distribution of tumor location was similar in two groups, so this should not have affected the outcome. In cases of lesser curvature lesions, axis deviation after partial gastrectomy might occur. Although the branches of the vagus nerve in the hepatogastric ligament are macroscopically preserved, the intramural branches may be injured or removed during mobilization, resection, and closure. These factors may be responsible for postoperative dysmotility of the gastric remnant, which results in this dysfunction. It is important to always consider conversion from straight laparoscopy to laparoscopy-assisted surgery to maintain gastric remnant function. Further studies – preferably multicenter, prospective, randomized trials – are necessary to confirm this explanation. In conclusion, although further evaluation is necessary, laparoscopic partial gastrectomy satisfactorily appears to preserve organ function when an adequate surgical technique is applied. Additional care is necessary for patients with lesser curvature lesions, as they have a higher risk of developing postoperative GI symptoms related to gastric remnant dysmotility.

Acknowledgments The authors have no conflicts of interest or financial ties to disclose.

References 1. Otani Y, Furukawa T, Yoshida M et al. Operative indications for relatively small (2–5 cm) gastrointestinal stromal tumor of the stomach based on analysis of 60 operated cases. Surgery 2006; 139: 484–492. 2. Nishimura J, Nakajima K, Omori T et al. Surgical strategy for gastric gastrointestinal stromal tumors: Laparoscopic vs. open resection. Surg Endosc 2007; 21: 875–878. 3. William G, Hawkins A, David C et al. Laparoscopic gastric resection for gastrointestinal stromal tumors. Surg Endosc 2008; 22: 2583–2587. 4. Demetri GD, Benjamin RS, Blanke CD et al. NCCN Task Force report: Management of patients with gastrointestinal stromal tumor (GIST)—update of the NCCN clinical practice guidelines. J Natl Compr Canc Netw 2007; 5 (Suppl 2): S1–29; quiz S30.

Asian J Endosc Surg 8 (2015) 24–28 © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd.

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5. Kubo M, Sasako M, Gotoda T et al. Endoscopic evaluation of the remnant stomach after gastrectomy: Proposal for a new classification. Gastric Cancer 2002; 5: 83–89. 6. Fletcher CD, Berman JJ, Corless C et al. Diagnosis of gastrointestinal stromal tumors: A consensus approach. Hum Pathol 2002; 33: 459–465.

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7. Bozzetti F, Marubini E, Bonfanti G et al. Total versus subtotal gastrectomy surgical morbidity and mortality rates in a multicenter Italian randomized trial. Ann Surg 1997; 226: 613– 620.

Asian J Endosc Surg 8 (2015) 24–28 © 2014 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and Wiley Publishing Asia Pty Ltd.

Clinical outcomes of laparoscopic partial gastrectomy for gastric submucosal tumors.

Laparoscopic partial gastrectomy has become a common procedure for gastric submucosal tumors because of its accepted feasibility, safety, and oncologi...
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