Introduction

Since Kitano et al. [1] reported the first laparoscopy-assisted gastrectomy for gastric cancer in 1991, this technique has become increasingly popular in Japan. Although laparoscopic distal gastrectomy is a popular choice of treatment for early gastric cancer, laparoscopic total gastrectomy (LTG) or proximal gastrectomy (LPG) is still uncommon. Indeed, 40.1% of all gastrectomies were being performed using conventional open techniques for total gastrectomy, whereas only 19.2% of these surgeries were laparoscopy assisted [2]. This may be attributed to the technical difficulty of performing laparoscopy-assisted esophagojejunostomy or esophagogastrostomy.

Circular staplers are frequently used during open esophagojejunostomy, and extensive efforts have been made to apply this device to laparoscopic surgery [3–8]. However, these procedures require additional small incisions to insert the circular stapler into the peritoneal cavity; in addition, there are some technical difficulties in handling the circular stapler and inserting the anvil head into the esophagus because of the limited working space.

Recently, Inaba and colleagues reported a novel method of intracorporeal esophagojejunostomy using a linear stapler after LTG, and they termed this procedure as the overlap method [9]. In this study, we evaluated the feasibility and safety of the overlap method for esophagojejunostomy or esophagogastrostomy after LTG or LPG, respectively.

Methods

Patients

A total of 98 patients with gastric cancer underwent laparoscopic gastrectomy at the Department of Surgery, National Defense Medical College Hospital, between 2008 and 2010. Of the total, 15 patients (15.3%) underwent LTG, and 10 (10.2%) underwent LPG. Anastomosis using a linear stapler during esophagojejunostomy and esophagogastrostomy was performed for all 25 patients after LTG and LPG, respectively.

The clinicopathological findings of the patients were evaluated on the basis of the Japanese Classification of Gastric Carcinoma (second English edition) published by the Japanese Gastric Cancer Association [10]. Gastric cancer staging was based on the preoperative assessment of depth of wall invasion, which was performed using upper gastrointestinal tract endoscopy, barium radiology, and endoscopic ultrasonography. Nodal involvement was determined by preoperative computed tomography [11].

Indication for LTG and LPG

Indications for all laparoscopic gastrectomies were as per those of the gastric cancer treatment guidelines in Japan [12], i.e., clinically mucosal or submucosal carcinoma without lymph node metastasis (cT1, cN0) was an indication for laparoscopic gastrectomy.

LPG was indicated for tumors in the upper part of the stomach and when more than half of the stomach could be preserved. LTG was indicated for tumors in the upper and/or middle thirds of the stomach and when tumors did not meet the criteria for LPG.

Anastomosis using a linear stapler during esophagojejunostomy and esophagogastrostomy

Following induction of general anesthesia, each patient was placed in a supine position. The surgeon was positioned on the left side of the patient, first assistant on the right, and the laparoscopist between the abducted legs of the patient. A camera port was inserted into a median umbilical incision. Next, a pneumoperitoneum of 12 mmHg was induced, and four additional ports (two ports with 12 mm diameter and two with 5 mm diameter) were inserted under laparoscopic imaging into the left upper, right lower, left lower, and right upper quadrants. An ultrasonically activated sealing device (Harmonic Scalpel Ace; Ethicon, Tokyo, Japan) and a vessel sealing device (Ligasure V; Tyco Healthcare, Tokyo, Japan) were used.

After gastrectomy was performed along with lymphadenectomy as per the tumor stage, a small opening was made in the right side of the esophagus where transection would occur (Fig. 1), following which mucosal and submucosal layers were sutured to the muscular layers with an absorbent monofilament suture (3-0 monocryl, Ethicon). The esophagus was transected with a 60-mm endoscopic linear stapler (Endo-GIA; Covidien, blue cartridge) (Fig. 2). The right diaphragmatic crus was partially divided using a vessel sealing device to widen the surgical field for reconstruction, if necessary. In total gastrectomy, tumors along with the surrounding tissues were pulled out through the umbilical trocar incision, which was extended by enlarging the median fascia and skin incision. Via a similar approach, in proximal gastrectomy, the upper third of the stomach and the surrounding tissue were drawn up.

Fig. 1
figure 1

Following gastrectomy with lymphadenectomy as per the tumor stage, a small opening is made on the right wall of the esophagus

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Fig. 2
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The exposed esophagus is transected with a 60-mm endoscopic linear stapler (Endo-GIA; Covidien, blue cartridge)

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During LTG, the jejunum was intracorporeally transected 20 cm distal to the ligament of Treitz using an Endo-GIA stapler (blue cartridge). The distal side of the jejunum (approximately 10 cm long) was additionally removed to avoid excessive tension at the site of anastomosis in esophagojejunostomy. A small enterotomy was made 7 cm distal to the stapler line on the antimesenteric side of the jejunal limb. After one fork of the 45-mm Endo-GIA stapler (blue cartridge) was inserted through this opening toward the oral side of the lumen, the jejunal limb was brought up to create an esophagojejunostomy in an antecolic fashion. Another fork of the linear stapler was inserted carefully into the hole of the esophagus under the guidance of a nasogastric tube (Fig. 3). After each fork was completely inserted into each lumen, the two limbs were mated to fashion the side-to-side esophagojejunal anastomosis (Fig. 4). A completion of esophagojejunal anastomosis and intraluminal hemostasis were then confirmed (Fig. 5). The entry hole of the stapler was closed using an intracorporeal interrupted hand-sewn technique with absorbable monofilament sutures (3-0 monocryl; Ethicon) (Fig. 6). Interrupted suturing was usually done 7–10 times, and the intracorporeal esophagojejunostomy anastomosis was completely established (Fig. 7). A jejunojejunostomy was performed using a previously reported procedure [13]. Closure was confirmed by laparoscopic examination after insufflating air into the jejunum and submerging the suture line in water. A closed suction drain (19 Fr J-VAC drain; Ethicon) was placed behind the esophagojejunostomy. A representative postoperative view of the surgical wound 6 months after LTG is shown in Fig. 8.

Fig. 3
figure 3

A small enterotomy is made 7 cm distal to the stapler line on the antimesenteric side of the jejunal limb. After one fork of the 45-mm Endo-GIA stapler (blue cartridge) is inserted through this opening toward the oral side of the lumen, another fork is inserted carefully into the hole of the esophagus under the guidance of a nasogastric tube

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Fig. 4
figure 4

An endoscopic linear stapler is inserted between the esophagus and jejunal limb. After each fork is completely inserted into each lumen, the stapler is fired to convert the two openings into a single entry hole to create a side-to-side esophagojejunostomy

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Fig. 5
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An anastomotic staple line is created between the esophagus and jejunal limb, and intraluminal hemostasis is confirmed

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Fig. 6
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The entry hole of the stapler is closed using an intracorporeal interrupted hand-sewn technique combined with extracorporeal Roeder's knots. An absorbent monofilament suture (3-0 monocryl; Ethicon) is used for suturing

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Fig. 7
figure 7

The intracorporeal esophagojejunostomy anastomosis is completely established

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Fig. 8
figure 8

Postoperative view of the surgical wound 6 months after LTG

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During LPG, the upper side of the stomach, which had an adequate surgical margin, was cut using a linear stapler (TL 90 mm; Ethicon), and a small gastrostomy was made 5 cm distal to the stapler line on the anterior wall of the stomach. An esophagogastrostomy was performed by the same procedure as described previously using a 45-mm Endo-GIA stapler. Fundoplication was performed as an antireflux procedure as previously described [14].

Statistical analysis

Statistical calculations were performed using StatView version 5.0 (SAS Institute, Inc., Cary, NC, USA). The data are expressed as mean ± standard deviation. Statistical analyses were performed using the Mann–Whitney U test or chi-square test with Fisher's exact test, whichever was considered appropriate. P values of <0.05 were considered statistically significant.

Results

The demographic data of patients who underwent LTG and LPG for early gastric cancer are depicted in Table 1. The average age of the patients was 69.3 years (range 40–88 years), and 19 of the 25 patients were male. The patients had an average body mass index (BMI) of 21.7 kg/m2 (range 13.8–31.9 kg/m2). All patients with tumors located in the middle part of the stomach underwent LTG; these patients had larger tumors and longer distal margin, and required extended lymphadenectomy, and a higher number of lymph nodes were harvested from these patients than that from patients who underwent LPG. The average surgical duration of LTG was 236.8 min (range 179–334 min), whereas that of LPG was 224.1 min (range 159–299 min) (Table 2). No difference was observed in the incidence of comorbidity between the two surgical procedures. Postoperative complications were observed in four patients (16.0%), of which one developed a wound infection and one developed an intestinal obstruction that required conservative therapy; after which, the patient was discharged on postoperative day (POD) 20. Of the remaining two, one developed afferent loop syndrome that was successfully treated by endoscopic drainage, and the patient was discharged on POD 42, and one LPG patient developed reflux symptoms that were treated by prolonged proton pump inhibitor therapy. In this patient, proximal esophageal resection was required because the tumor involved the distal esophagus. The average postoperative hospital stay of the patients was 12.5 days (range 7–42 days). No cases of conversion to open surgery, anastomotic leakage or stenosis, or mortality were observed.

Table 1 Demographic data of the patients who underwent LTG and LPG. BMI body mass index, U upper third of the stomach, M middle third of the stomach, L lower third of the stomach, LTG laparoscopic total gastrectomy, LPG laparoscopic proximal gastrectomy, LN lymph node
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Table 2 Surgical outcomes of the patients who underwent LTG and LPG. LTG laparoscopic total gastrectomy, LPG laparoscopic proximal gastrectomy. aOne patient had a history of two comorbidities
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Tumor recurrence during a mean follow-up period of 18.9 months (range 6–28 months) was not observed in any patient.

Previous reports describing surgical outcomes of esophagojejunostomy or esophagogastrostomy using laparoscopic staplers after LTG or LPG, respectively, are shown in Table 3 [15–19].

Table 3 Previous reports describing the surgical outcomes of esophagojejunostomy or esophagogastrostomy using laparoscopic staplers. LPG laparoscopic proximal gastrectomy, LTG laparoscopic total gastrectomy, NR not referred
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Discussion

In this study, we demonstrated the safety and feasibility of anastomosis using the overlap method during esophagojejunostomy and esophagogastrostomy after LTG and LPG, respectively.

In conventional open total gastrectomy, esophagojejunal and esophagogastric anastomoses are mostly performed using circular stapling devices. According to previous reports, esophagojejunostomy after LTG has also been performed using circular staplers to reproduce the results of open surgery [3, 6, 20, 21]. However, there are still potential problems in performing these procedures with a circular stapling device. Placing a purse-string suture in the distal esophagus and inserting an anvil head are occasionally problematic because the esophagus is shortened after it is transected, which may lead to disruption of the esophageal wall. In addition, this procedure requires 3–6 cm of additional minilaparotomy to insert the circular stapler into the peritoneal cavity (Table 3) [3, 21–24]. In the anastomosis presented here, minilaparotomy for esophagojejunostomy or esophagogastrostomy was not necessary, and it was easy to confirm the intraluminal hemostasis after the first firing of the stapler.

We believe that there are two factors that contribute to the successful achievement of this anastomosis. First, a small opening of the esophagus was made before transection of the esophagus. As mentioned previously, the esophagus is shortened after it is transected, and it is also difficult to maintain sufficient tension for making a small enterotomy. Second, we put a single suture through all the layers so that there were no gaps between the submucosal and muscular layers. This facilitated adequate insertion of the stapler into the esophageal lumen to lift the distal esophagus after transection (Fig. 2).

In this study, no case required conventional open surgery, and no technical difficulties were encountered while achieving anastomosis using these procedures. Even with obese patients (BMI > 25), we did not encounter any difficulties during the surgeries, and there was no difference in the duration of surgeries between patients with high and low BMI (BMI > 25: 246.2 ± 59.0 min, BMI ≤ 25: 227.0 ± 35.9 min, respectively). Furthermore, no patients with BMI > 25 had postoperative complications. These findings suggest that this procedure is not affected by intraabdominal and subcutaneous fat.

If a tumor involves the distal esophagus and/or is an advanced esophagogastric cancer, peritoneal seeding may occur [25]. In these cases, therefore, resection of the esophagus must be performed without an enterotomy before the transection of the esophagus [9].

The results of this study are comparable to those of previous studies in terms of surgical duration, hospitalization, and incidence of leakage and stenosis (Table 3). In this context, the overlap method using a linear stapler for esophagojejunostomy or esophagogastrostomy after LTG or LPG, respectively, is safe and feasible; in addition, it provides satisfactory outcomes. This procedure does not require an additional minilaparotomy, which may result in less pain and favorable cosmetic outcomes. We believe that this procedure will facilitate the acceptance of LTG and LPG as surgical options for patients with early proximal gastric cancer.