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 Table of Contents     
Year : 2018  |  Volume : 14  |  Issue : 3  |  Page : 236-240

Stomach resection with intraoperative fluoroscopy in laparoscopic distal gastrectomy for early gastric cancer

1 Department of Surgery, Shonan Kamakura General Hospital, Kamakura, Japan
2 Gastroenterology Center, Shonan Kamakura General Hospital, Kamakura, Japan
3 Department of Surgery, Shonan Atsugi Hospital, Atsugi, Japan
4 Department of Pathology, Shonan Kamakura General Hospital, Kamakura, Japan
5 Department of Surgery, Tokyo Nishi Tokushukai Hospital, Tokyo, Japan

Date of Submission30-Mar-2017
Date of Acceptance14-Sep-2017
Date of Web Publication6-Jun-2018

Correspondence Address:
Dr. Jun Kawachi
Department of Surgery, Shonan Kamakura General Hospital, Kamakura
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmas.JMAS_61_17

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 ¤ Abstract 

Background: In Japan, laparoscopic distal gastrectomy (LDG) is common for early gastric cancer. Formerly, we used to verify the location of the marking clip to decide the proximal incisional line with our hand, through a small epigastric incision. In 2015, we introduced intracorporeal reconstruction and started to decide the incisional line using intraoperative fluoroscopy. Herein, we aimed to evaluate the efficacy and safety of intraoperative fluoroscopy in LDG.
Patients and Methods: A total of 19 patients were included in this retrospective observational study. On the day before operation, we endoscopically clipped several points located 2 cm proximal to the tumour edge to cover about half of the tumour. After lymph node dissection, we incised the stomach with an endoscopic linear stapling device, including the previously placed clips, guided by intraoperative fluoroscopy. Reconstruction was performed in all patients who underwent Billroth I and Roux-en-Y procedures.
Results: No complications were observed during pre-operative endoscopic clipping or intraoperatively. On pathological examination, all resected specimens had negative margins, and the mean distance from the tumour edge was 28.5 ± 16.5 (13–60) mm.
Conclusion: Stomach resection with intraoperative fluoroscopic guidance was safe and effective.

Keywords: Early gastric cancer, intraoperative fluoroscopy, laparoscopic distal gastrectomy

How to cite this article:
Kawachi J, Kashiwagi H, Ogino H, Isogai N, Shimoyama R, Fukai R, Miyake K, Sasaki A, Terashima T, Teshima S, Watanabe K. Stomach resection with intraoperative fluoroscopy in laparoscopic distal gastrectomy for early gastric cancer. J Min Access Surg 2018;14:236-40

How to cite this URL:
Kawachi J, Kashiwagi H, Ogino H, Isogai N, Shimoyama R, Fukai R, Miyake K, Sasaki A, Terashima T, Teshima S, Watanabe K. Stomach resection with intraoperative fluoroscopy in laparoscopic distal gastrectomy for early gastric cancer. J Min Access Surg [serial online] 2018 [cited 2022 Jan 24];14:236-40. Available from:

 ¤ Introduction Top

Recently, laparoscopic surgery for early gastric cancer is increasingly being performed [1] and shows good oncological outcome.[2] Compared with open surgery, laparoscopic surgery provides a better quality of life.[3] As for distal gastrectomy, the trend is changing from laparoscopy-assisted distal gastrectomy (LADG) to laparoscopic distal gastrectomy (LDG), in which gastrointestinal anastomosis is performed intracorporeally. LDG is less invasive than LADG.[4],[5] Delineation of the proximal incision line is the key for distal gastrectomy. In the era of LADG, direct contact with the clips placed pre-operatively is possible through a small epigastric wound. In LDG, direct contact with the clips is not possible because of intra-abdominal reconstruction. Although several methods for identification of the tumour have been suggested, it is unclear which method is the best. This study aimed to evaluate the efficacy and safety of intraoperative fluoroscopy to identify the clips placed pre-operatively to delineate the proximal resection line during LDG.

 ¤ Patients and Methods Top

From January 2015 to December 2016, retrospective review of 19 patients who underwent LDG under intraoperative fluoroscopic guidance was performed. The inclusion criterion was tumour stage T1N0M0. Patients with advanced gastric cancer, lymph node metastasis, and those requiring additional resection post-endoscopic submucosal dissections were excluded.

The institutional ethics committee approved this study, allowing patients to opt-out instead of providing informed consent.

Pre-operative marking

On the day before operation, several clips (HX-600-090 L, Olympus, Tokyo) were endoscopically placed at 2 cm from the tumour edge to cover its proximal half [Figure 1].
Figure 1: Endoscopic pre-operative clipping

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Operative details

Under general and epidural anaesthesia, LDG was performed with 5 ports (two 12-mm trocars and three 5-mm trocars). After lymph node dissection and incision of the duodenum, the C-arm (OEC 9900 Elite, GE Healthcare UK Ltd, Little Chalfont, Buckinghamshire, England) was positioned as shown in [Figure 2]. Surgeons, nurses, and anaesthesiologists were shielded with protectors. The proximal gastric incision line was marked with 1% Crystal violet on the serosal surface of the stomach, with the aid of clips under fluoroscopic guidance, followed by incision with a linear stapling device (Endo GIA™ 60 mm Reload with Tri-Staple™ Technology, Medtronic plc, Dublin, Ireland), using 2 or 3 cartridges from the left lower port [Figure 3] and [Figure 4]. After removal of the stomach through the small umbilical incision and confirming that all clips were included in the resected stomach [Figure 5], intracorporeal gastrointestinal reconstruction was performed. Billroth I (B-I) or Roux-en-Y (R-Y) method was selected, depending on the size of the remnant stomach. As for R-Y reconstruction, jejunojejunostomy was performed extracorporeally through the small umbilical incision. D1+ lymph node dissection was done, according to the Japanese guideline for gastric cancer.[6]
Figure 2: C-arm setting during operation

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Figure 3: Stomach resection with linear stapling device

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Figure 4: Resection under intraoperative fluoroscopy

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Figure 5: Resected specimen with clips

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All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Japan, version 1.32), which is a graphical interface for R, version 3.2.2 (The R Foundation for Statistical Computing, Vienna, Austria). For continuous variables, we calculated descriptive statistics, including the number of patients, mean and standard deviation, minimum, maximum and median. Student's t-test and one-way analysis of variance were used for comparing means. A two-tailed P = 0.05 was considered statistically significant.

 ¤ Results Top

The mean age of the 19 patients (8 men and 11 women) was 68.2 ± 13 years [Table 1]. No complications were observed during pre-operative clipping. The mean operative time (11 B-I and 8 R-Y) was 275.5 ± 38.5 min, and the mean blood loss was 34.4 ± 38.4 ml. Mean length of hospital stay was 12.8 ± 2.6 days. Complications included wound infection (n = 1), paralytic ileus (n = 1) and delayed gastric empting (n = 1), which were managed conservatively.
Table 1: Demographic and clinical characteristics of patients

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Although the indication for operation was T1N0M0, more advanced cases (pT2: n = 3, pT3: n = 2, and pT4: n = 1) were seen. The mean longest-diameter of the tumour was 37.8 ± 25.4 mm. The margins of all resected specimens were negative, and the mean proximal-margin length was 28.5 ± 16.5 (range: 13 − 60) mm.

Tumour size [≧40 mm, ≦30 mm, [Figure 6], differentiation [differentiated, undifferentiated: [Figure 7], and depth [pT1a, pT1b, ≦ pT2: [Figure 8] were not associated with tumour margins, respectively.
Figure 6: Size and margin

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Figure 7: Differentiation and margin

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Figure 8: Depth and margin

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 ¤ Discussion Top

The trend in surgery for early gastric cancer is shifting from LADG to LDG.[7] We had been performing LADG since 2008. We manually check for the correct location of clips around a tumour through a small epigastric incision. Since 2015, we have been performing LDG, which comprises intracorporeal gastrointestinal reconstruction. At first, we used Chinese ink that was endoscopically injected pre-operatively to delineate the proximal incision line. However, the ink was sometimes invisible or too widely distributed. Then, we surmised that intraoperative fluoroscopy might be useful to identify clips that were endoscopically placed pre-operatively to obtain an oncological safety margin. In this study, all resected specimens had negative margins. In the Japanese guidelines for gastric cancer, a margin >2 cm for T1 cancer is recommended. In this study, we placed the clips 2 cm from the proximal edge pre-operatively. The mean pathological margin was 28.5 mm, which was considered adequate.

A negative margin is important in distal gastrectomy because it affects local recurrence and prognosis.[8],[9] Many methods of identifying a tumour have been reported, including methylene blue injection,[10] indigo carmine injection,[11] intraoperative laparoscopic ultrasonography,[12] intraoperative portable radiography,[13] and intraoperative endoscopy.[14],[15] Intraoperative endoscopic determination of a resection line with adequate margin may sometimes be difficult for the surgeon. We believe it is better for the endoscopist to determine the incision line in a properly equipped room, especially for undifferentiated early cancers. Intraoperative ultrasonography requires practice, and intraoperative endoscopy requires adequate space for instruments to be placed near the anaesthesiologist. Our method is simple and easy. Moreover, C-arms are usually used in operating rooms.

Study limitation

This was a retrospective observational study with a small sample size. An additional disadvantage of this method is radiation exposure. Unfortunately, this was not investigated in this study. The duration of radiation exposure was about 30 s, and the organ dosage was about 3 or 4 mGy. Surgeons, scrub nurses and anaesthesiologists were shielded with protectors. As for the patient, the field was limited around the stomach. We believe that this is not excessive exposure when obtaining a safe oncological margin, but further studies are needed.

In conclusion, intraoperative fluoroscopy with pre-operative clipping is simple, easy and effective and enables determination of the proper proximal resection line for LDG. Further, studies should be conducted to evaluate radiation exposure in comparison with other methods.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 ¤ References Top

Noh SH, Hyung WJ, Cheong JH. Minimally invasive treatment for gastric cancer: Approaches and selection process. J Surg Oncol 2005;90:188-94.  Back to cited text no. 1
Kitano S, Shiraishi N, Uyama I, Sugihara K, Tanigawa N; Japanese Laparoscopic Surgery Study Group. A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg 2007;245:68-72.  Back to cited text no. 2
Yasuda K, Shiraishi N, Etoh T, Shiromizu A, Inomata M, Kitano S. Long-term quality of life after laparoscopy-assisted distal gastrectomy for gastric cancer. Surg Endosc 2007;21:2150-3.  Back to cited text no. 3
Song KY, Park CH, Kang HC, Kim JJ, Park SM, Jun KH, et al. Is totally laparoscopic gastrectomy less invasive than laparoscopy-assisted gastrectomy?: Prospective, multicenter study. J Gastrointest Surg 2008;12:1015-21.  Back to cited text no. 4
Kinoshita T, Shibasaki H, Oshiro T, Ooshiro M, Okazumi S, Katoh R. Comparison of laparoscopy-assisted and total laparoscopic Billroth-I gastrectomy for gastric cancer: A report of short-term outcomes. Surg Endosc 2011;25:1395-401.  Back to cited text no. 5
Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver 4). Gastric Cancer 2017;20:1-19.  Back to cited text no. 6
Etoh T, Yasuda K, Inomata M, Shiraishi N, Kitano S. Current status of laparoscopic gastrectomy for gastric malignancies. Surg Technol Int 2010;20:153-7.  Back to cited text no. 7
Woo JW, Ryu KW, Park JY, Eom BW, Kim MJ, Yoon HM, et al. Prognostic impact of microscopic tumor involved resection margin in advanced gastric cancer patients after gastric resection. World J Surg 2014;38:439-46.  Back to cited text no. 8
Morgagni P, Garcea D, Marrelli D, De Manzoni G, Natalini G, Kurihara H, et al. Resection line involvement after gastric cancer surgery: Clinical outcome in nonsurgically retreated patients. World J Surg 2008;32:2661-7.  Back to cited text no. 9
Beretvas RI, Ponsky J. Endoscopic marking: An adjunct to laparoscopic gastrointestinal surgery. Surg Endosc 2001;15:1202-3.  Back to cited text no. 10
Xuan Y, Hur H, Byun CS, Han SU, Cho YK. Efficacy of intraoperative gastroscopy for tumor localization in totally laparoscopic distal gastrectomy for cancer in the middle third of the stomach. Surg Endosc 2013;27:4364-70.  Back to cited text no. 11
Hyung WJ, Lim JS, Cheong JH, Kim J, Choi SH, Song SY, et al. Intraoperative tumor localization using laparoscopic ultrasonography in laparoscopic-assisted gastrectomy. Surg Endosc 2005;19:1353-7.  Back to cited text no. 12
Kim HI, Hyung WJ, Lee CR, Lim JS, An JY, Cheong JH, et al. Intraoperative portable abdominal radiograph for tumor localization: A simple and accurate method for laparoscopic gastrectomy. Surg Endosc 2011;25:958-63.  Back to cited text no. 13
Matsui H, Okamoto Y, Nabeshima K, Kondoh Y, Ogoshi K, Makuuchi H. Endoscopy-assisted gastric resection: A safe and reliable procedure for tumor clearance during laparoscopic high distal or proximal gastrectomy. Surg Endosc 2009;23:1146-9.  Back to cited text no. 14
Gunji H, Horibe D, Uesato M, Kano M, Hayano K, Hanari N, et al. Gastric resection under retroflexed endoscopic guidance: A reliable procedure for totally laparoscopic subtotal gastrectomy. Dig Surg 2017;34:12-7.  Back to cited text no. 15


  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]

  [Table 1]


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