In early gastric cancer, the aim of surgery is to precisely remove the distal stomach including the primary tumor. To do this, accurate localization of the tumor is crucial, especially in totally laparoscopic surgery. This protocol describes a procedure for intraoperative gastroscopy in totally laparoscopic subtotal gastrectomy.
Determining resection margins for gastric cancer, which are not exposed to the serosal surface of the stomach, is the most important procedure during totally laparoscopic gastrectomy (TLG). The aim of this protocol is to introduce a procedure for intraoperative gastroscopy, in order to directly mark tumors during TLG for gastric cancer in the middle third of the stomach. Patients who were diagnosed with adenocarcinoma in the middle third of the stomach were enrolled in this case series. Before surgery, additional gastroscopy for tumor localization is not performed. Under general anesthesia, laparoscopic mobilization of the stomach is performed first. After the first portion of the duodenum is mobilized from the pancreas and clamped, the surgeon moves to the other side for the gastroscopic procedure. On the insertion of a gastroscope through the oral cavity into the stomach, 2 – 3 cc of indigo carmine is administered via an endoscopic injector into the gastric muscle layer at the proximal margin of the stomach. The location of stained serosa in the laparoscopic view is used to guide distal subtotal gastrectomy, however, total gastrectomy is performed if the tumor is too close to the esophagogastric junction. A specimen is sampled after distal gastrectomy to confirm sufficient length from resection margin to tumor before reconstruction. In our case series, all patients had tumor-free margins and required no additional resection. There was no morbidity related to the gastroscopic procedure, and the time required for the procedure has gradually decreased to about five minutes. Intraoperative gastroscopy for tumor localization is an accurate and tolerated method for gastric cancer patients undergoing totally laparoscopic distal gastrectomy.
Laparoscopic surgery has been become the treatment of choice for early gastric cancer in East Asian countries, including Korea and Japan.1 The advantage of this surgery has been well demonstrated in several clinical trials for early gastric cancer (EGC).2-4 Most of the procedures in these trials were accomplished by laparoscopy, but identification of the tumor location, resection of the stomach, including the primary tumor, and reconstruction were performed via minilaparotomy. Therefore, surgery requiring minilaparotomy has been labeled "laparoscopy-assisted gastrectomy."
Recently, however, surgical procedures have evolved to minimize trauma, improving the postoperative quality of life for patients. Since this concept has also been applied in laparoscopic surgery for gastric cancer, some experienced laparoscopic surgeons have tried to avoid minilaparotomy. Totally laparoscopic gastrectomy (TLG) for gastric cancer requires that all procedures are completed using only laparoscopic devices, without requiring an additional minilaparotomy for specimen resection and anastomosis. Since this type of surgery results in less pain and faster recovery relative to open or laparoscopy-assisted surgery, which require laparotomy, more surgeons prefer it.5,6 However, an obstacle to TLG for gastric cancer is tumor localization without direct visualization or palpation to determine the area of stomach resection.
Tumor absence at the resection margin is very important to achieve success in gastric cancer surgery. If there is tumor involvement at the resection margin during distal gastrectomy for gastric cancer, additional resection is needed to avoid leaving tumor in the remaining stomach. In open and laparoscopy-assisted surgery, the primary tumor can be easily localized by palpation or direct visualization through a temporary gastrostomy. However, because the primary tumor is not easily detected in the laparoscopic view, determining resection margins for EGC in TLG may be difficult.
Several other methods requiring additional preoperative gastroscopy to determine resection margins have been proposed.7-9 However, additional preoperative gastroscopy can be inconvenient for patients. We introduced a procedure for intraoperative gastroscopy to directly mark tumors during TLG for gastric cancer in the middle third of the stomach.
In this protocol, we applied the laparoscopic surgery for patients with early gastric cancers at the preoperative studies, which are not included in absolute indication for endoscopic submucosal dissection.
Ethics Statement: This procedure involving human subjects has been approved by the Institutional Review Board (IRB) at Ajou University Hospital.
1. Preparation for Surgery
2. Surgical Procedure before Intraoperative Gastroscopy
3. Intraoperative Gastroscopy
4. Procedure after Intraoperative Gastroscopy
5. Procedure after Intraoperative Gastroscopy
Of 20 patients who underwent intraoperative gastroscopy, 18 underwent distal subtotal gastrectomy, guided by findings at gastroscopy. However, we performed total gastrectomy on two patients, because the proximal tumor margin was too close to the esophagogastric junction, as determined on intraoperative gastroscopy. The distance from the tumor to the proximal resection margin was 3.5 cm and 2.5 cm in these two patients, respectively (Table 1).
Total mean operative time for distal gastrectomy was 188 min. The mean time for tumor localization with intraoperative gastroscopy was 8.4 min, and it gradually decreased from 11.8 min (initial 5 cases) to 4.6 min (last 5 cases) (Figure 5). Intracorporeal reconstruction with Billroth II anastomosis followed distal gastrectomy in all patients. There was no morbidity, except for gastric stasis and adhesive ileus in two patients. Finally, there were no complications related to intraoperative gastroscopy.
Mean tumor size in patients who underwent distal gastrectomy was 2.89 (range: 0.5 – 3.2) cm. EGC was the final diagnosis in 16 patients, but one exhibited muscle invasion and another exhibited serosal invasion. The mean distance from tumor to resection margin was 3.3 (range: 0.5 – 6.7) cm. Most common histologic type was signet ring cell carcinoma (Table 1).
No. | Age, y | Sex | LNa dissect- ion |
Resect- ion |
Recon- struction |
Opb time, min | GFSc time, min | Location | Frozen for PRMd | Histo- logy |
Stage | Tumor size, cm | Proximal length from tumor, cm |
1 | 57 | male | D1+ | Subtotal | Billroth-II | 235 | 15 | Posterior | Tumor free | signet ring cell | Ia | 2.5 | 2.7 |
2 | 44 | female | D2 | Subtotal | Billroth-II | 140 | 12 | Greater | Tumor free | signet ring cell | Ia | 1 | 6 |
3 | 51 | female | D2 | Subtotal | Billroth-II | 195 | 10 | Posterior | Tumor free | signet ring cell | Ia | 1 | 7 |
4 | 34 | female | D2 | Subtotal | Billroth-II | 235 | 10 | Anterior | Tumor free | Pooly differen- tiated |
Ia | 1.5 | 6.7 |
5 | 56 | male | D2 | Subtotal | Billroth-II | 225 | 12 | Greater | Tumor free | signet ring cell | Ia | 1.5 | 3 |
6 | 51 | male | D1+ | Subtotal | Billroth-II | 200 | 13 | Lesser | Tumor free | Moderatly differen- tiated |
Ia | 2 | 4.1 |
7 | 46 | female | D1+ | Subtotal | Billroth-II | 110 | 8 | Greater | Tumor free | signet ring cell | Ia | 2 | 4 |
8 | 68 | female | D2 | Subtotal | Billroth-II | 200 | 7 | Lesser | Tumor free | Pooly differen- tiated |
Ib | 5 | 2 |
9 | 42 | female | D1+ | Subtotal | Billroth-II | 170 | 9 | Lesser | Tumor free | signet ring cell | Ib | 3.2 | 3.6 |
10 | 50 | male | D1+ | Subtotal | Billroth-II | 200 | 12 | Lesser | Tumor free | signet ring cell | Ia | 2.5 | 0.5 |
11 | 31 | female | D1+ | Subtotal | Billroth-II | 210 | 8 | Greater | Tumor free | signet ring cell | Ia | 1.2 | 1.3 |
12 | 56 | female | D2 | Subtotal | Billroth-II | 175 | 7 | Lesser | Tumor free | signet ring cell | IIIa | 2.5 | 0.5 |
13 | 65 | male | D1+ | Subtotal | Billroth-II | 150 | 5 | Lesser | Tumor free | Undiffer- entiated |
Ia | 0.5 | 5 |
14 | 36 | female | D1+ | Total | Roux-en-Y | 180 | Conver- sion |
Lesser | Tumor free | signet ring cell | IIa | 1.5 | 3.5 |
15 | 71 | female | D1+ | Subtotal | Billroth-II | 190 | 5 | Greater | Tumor free | signet ring cell | Ia | 11 | 2.6 |
16 | 48 | female | D2 | Subtotal | Billroth-II | 185 | 4 | Anterior | Tumor free | signet ring cell | Ia | 6 | 1.3 |
17 | 36 | female | D1+ | Total | Roux-en-Y | 305 | Conver- sion |
Greater | Tumor free | Pooly differen- tiated |
Ia | 7 | 2.5 |
18 | 46 | male | D1+ | Subtotal | Billroth-II | 180 | 4 | Posterior | Tumor free | Pooly differen- tiated |
Ia | 0.5 | 3 |
19 | 51 | male | D1+ | Subtotal | Billroth-II | 180 | 6 | Anterior | Tumor free | Well differen- taited |
Ia | 2 | 2.5 |
20 | 43 | female | D1+ | Subtotal | Billroth-II | 120 | 5 | Greater | Tumor free | signet ring cell | Ia | 0.6 | 7 |
Table 1: Surgical and Pathologic Outcomes of Patients who Underwent Intraoperative Gastroscope to Identify Tumor Location. Please click here to download this table.
Figure 1: Laparoscopic Clamp to Prevent Gas Passage into the Small Bowel. Before insertion of the gastroscope during surgery, the duodenum or jejunum should be clamped with a laparoscopic instrument. Gastroscopic procedures inevitably require the insufflation of gas into the lumen of the bowel to precisely visualize the lesions, and gas that has passed into the small bowel cannot be easily aspirated when the gastroscopic procedure finishes. Consequently, inflated small bowel can interfere with the laparoscopic procedure. Please click here to view a larger version of this figure.
Figure 2: Measurement of the Distance between the Tumor and Esophagogastric Junction. Most gastroscopes have a scale with approximate 5 cm gradations. If the distance between the margin of tumor and esophagogastric junction is 5 cm or less, it is too difficult to retain the proximal part of the stomach and the surgeon should perform a total gastrectomy for gastric cancer. Please click here to view a larger version of this figure.
Figure 3: Injection of Blue Dye into the Gastric Wall. A) An endoscopic injector can be introduced through a small channel on the gastroscope. The needle of the endoscopic injector is exposed, and injected into the gastric wall at an area 2 – 3 cm proximal from the tumor margin. If the needle is inserted into the gastric wall forcefully, it can penetrate the gastric wall, and the dye will be injected into the peritoneal cavity. B) This would make identification of the precise location of the tumor difficult in the laparoscopic view. Therefore, this injection procedure should be performed carefully. Please click here to view a larger version of this figure.
Figure 4: Laparoscopic Resection Guided by the Stained Surface of the Stomach. After lymph node dissection, the stomach should be resected at the proper area to completely remove the primary tumor. A) A marker made with a laparoscopic clip, which can be useful in determining the portion for resection, should be applied 5 to 10 min after gastroscopic injection of the dye. B) Laparoscopic resection can be completed with two or three laparoscopic linear staplers. Please click here to view a larger version of this figure.
Figure 5: Change in Time Required for Intraoperative Gastroscopy and Tumor Localization. The mean time for tumor localization with intraoperative gastroscopy (8.4 min) gradually decreased from 11.8 min (initial 5 cases) to 4.6 min (last 5 cases).
In this protocol, we introduced a procedure for intraoperative gastroscopy to accurately and reliably identify tumor location in the middle third of the stomach. We were able to successfully perform distal subtotal gastrectomy based on the findings of intraoperative gastroscopy.
To date, various methods have been applied to identify the location of early gastric cancer in the laparoscopic view. Most common methods used preoperative gastroscopic clipping, and surgeons could detect the location of clips using laparoscopic ultrasonography or portable plain radiography.7,9 These techniques required additional preoperative gastroscopy one or two days before surgery. Laparoscopic ultrasonography for intraoperative detection of clips requires specific instruments and skills and involves subjective interpretation. Another option, intraoperative portable radiology, can show only a two-dimensional view; additional exposure to radiation can be harmful to patients. Recently, Jeong and colleague reported gastroscopic autologous blood tattooing before surgery.8 They reported that this procedure also requires preoperative gastroscopy one day before surgery, and consequently is inconvenient for patients. Another disadvantage of this procedure is that it is impossible to recognize incorrect injection into the gastric wall before surgery.
Unlike other procedures, we performed additional gastroscopy while patients were under general anesthesia during surgery. Therefore, patients enrolled in the present study avoided the inconvenience of additional preoperative gastroscopy. The dye injected into the muscle layer was easily detected during surgery, because we examined the serosa within 5 to 10 min after injection, and immediately clipped the center of the stained serosa before the dye spread. The exact tumor location was detected in all patients with our procedure.
The critical step of our procedure is injection of the blue dye into the gastric wall without leakage into the extraluminal area. When more commonly used dyes, such as methylene blue, leak into the intraperitoneal region, there is concern for the occurrence of postoperative adhesions, methemoglobinemia, and pulmonary edema by chromopertubation. In our protocol, indigo carmine is used instead of methylene blue, because it is a relatively nontoxic, inexpensive dye. Even so, the leakage of dye can make precise localization of tumors difficult. Therefore, it is recommended that a surgeon experienced in gastroscopic procedures, such as endoscopic injection, perform this procedure.
When blue dye and a specific instrument like an endoscopic injector are not available, our procedure can be modified. As soon as the operating surgeon inserts the gastroscope and inflates the stomach, the assistant surgeon compresses the area where the primary tumor is expected to be located, enabling the operating surgeon to identify the distance between the location of the primary tumor and the compressed lesion. Through communication between the operating and the assistant surgeon, the tumor can be precisely localized.
Several limitations of our technique for tumor localization should be considered. First, intraoperative gastroscopy may require a learning curve for specific endoscopic skills. One report suggested that surgeons would overcome the learning curve of gastroscopic procedures after about 80-90 cases.12 The surgeon who participated in this study had sufficient experience (more than 400 cases) to overcome the learning curve. Sometimes, intraoperative gastroscopy may be difficult due to the positioning of patients under general anesthesia. If the anesthesiologist extends the jaw of the patient, the gastroscope can be easily passed through the throat and into the esophagus. Second, specific devices for this procedure, like the gastroscopic system, should be ready in the operating room. However, several recently suggested procedures for gastric resection also require use of an intraoperative gastroscope.13,14 In the future, intraoperative gastroscopy will be more common in gastric surgery, and the gastroscopic system will be essential in the operating room Third, tumor margins were only determined by endoscopic findings in this protocol. Sometimes, the margin of superficial spreading tumors can be unclear, even though an elevated and discolored lesion can be assumed to be a tumor. Recent evolving techniques, such as infrared endoscopy or molecular in vivo imaging, may verify the tumor margin; if applied to intraoperative gastroscopy,15,16 the procedure in this protocol can be more accurate and useful.
In conclusion, intraoperative gastroscopy for tumor localization is an accurate and tolerated method for gastric cancer patients undergoing totally laparoscopic distal gastrectomy.
The authors have nothing to disclose.
This study was supported by a grant from the National R&D Program for Cancer Control, Ministry of Health & Welfare, Republic of Korea (1320270).
Pentothal Sodium | JW pharmatheutical Co. | 644912100 | It was used as induction asgent |
Rocumeron | Ilsung pharmatheutical Co. | 655402960 | It was used for general anesthestia as muscle relaxant. |
SevoFRAN | Hana pharmatheutical Co. | 657801060 | It was used as general anesthetics |
Endoscopy system | Olympus Corp. | CLV-260 | It was used for intraoperative GFS |
Laparoscopic surgery system | Striker Endoscopy | 1488 HD 3-CHIP | It was a system for laparoscopic surgery |
Ultrasonic scissor | Johnson and Johnson Medical Corp. | HAR23 | It was used during tissue dissection |
Laparoscopic clip | Johnson and Johnson Medical Corp. | ER420 | It was used for ligation of the vessels. |
Indigo carmine | Korea United Pharma | Carmine | It was injected into the gastric wall |
Linear stapler | Johnson and Johnson Medical Corp. | ECHELON FLEX Powered Endopath Stapler | It was used for resection the stomach |
Gastroscopic injector | TaeWoong Medical | Cobra injector | I was used for gastroscopic injection of blue dye |