Practicality and short-term outcomes of intracorporeal gastroduodenostomy in totally laparoscopic distal gastrectomy for gastric cancer: A single-centre retrospective study.

OBJECTIVE: Totally laparoscopic distal gastrectomy (TLDG) with intracorporeal anastomosis is feasible because of improved approaches to laparoscopic surgery and the availability of a variety of surgical instruments. This study was designed to evaluate the practicality, safety and short-term operative outcomes of intracorporeal gastroduodenostomy in TLDG for gastric cancer.
MATERIALS AND METHODS: Medical records of patients with primary distal gastric cancer undergoing Billroth I (B-I) (n = 37) or B-II anastomosis (n = 41) in TLDG from February 2010 to November 2015 were retrospectively analysed. Perioperative data including the extent of lymph node dissection, number of stapler cartridges used, time required to create the anastomosis, operative time, estimated blood loss, proximal and distal margin length, and number of lymph nodes harvested were collected. Short-term post-operative outcomes evaluated during the initial 30 days after surgery included time to first flatus and earliest liquid consumption, length of post-operative hospital stay and incidence of post-operative complications.
RESULTS: B-I anastomosis was mainly applied to patients with carcinoma in the lower third of the gastric body (B-I, 81.08% vs. B-II, 31.71%;P < 0.001). Mean operating (B-I, 153.57 ± 18.25 min vs. B-II, 120.17 ± 11.74 min;P = 0.004) and anastomosis (B-I, 31.92 ± 6.10 min vs. B-II, 25.29 ± 3.84 min;P = 0.01) times were significantly longer for B-I anastomosis compared to B-II anastomosis. There were no significant differences in the number of stapler cartridges used, estimated blood loss, time to first flatus and liquid consumption, length of hospital stay or incidence of complications between these groups.
CONCLUSIONS: TLDG with B-I or B-II anastomosis is safe and feasible for gastric cancer. B-II anastomosis may require less time than B-I anastomosis.

INTRODUCTION

Laparoscopy-assisted gastrectomy (LAG) for gastric cancer has become technically advanced and gained increasing popularity since it was introduced by Kitano et al. in 1994.[1] Due to rapid developments in surgical instrumentation and increased surgeon experience with the technique, LAG has become an accepted treatment option for advanced gastric cancer. LAG generally requires an epigastrium auxiliary incision where the stomach is exteriorised for resection and anastomosis. The advantages of LAG, including less cosmetic disfigurement, shorter hospitalisation, reduced post-operative pain and better quality of life, are universally acknowledged.[23] However, this technique is associated with some challenges. Performing gastrojejunostomy through a small incision is difficult due to poor visualisation and limited space. Furthermore, evidence suggests that extracorporeal anastomosis can easily cause tissue traction and injury, as well as infection.[45] As laparoscopic surgery techniques and instruments have evolved, the totally laparoscopic approach is being used for intracorporeal anastomosis at experienced laparoscopic centres. The advantages of totally laparoscopic distal gastrectomy (TLDG) include better visualisation for a safer anastomosis, decreased tissue trauma and more rapid post-operative recovery.[678] Patient outcomes are affected by the intracorporeal anastomotic procedures used for reconstruction in TLDG. Similar to conventional laparotomy, these procedures include Billroth I (B-I) (delta-shaped) anastomosis, B-II anastomosis and Roux-en-Y (RY) reconstruction. The benefits of these different methods for intracorporeal anastomosis in TLDG are often assumed but have not been confirmed, and studies comparing the efficacy and safety of the different anastomotic procedures are scarce. Therefore, we conducted this single-centre retrospective study to compare the practicality, safety and short-term operative outcomes of different methods of intracorporeal anastomosis in TLDG for gastric cancer.

MATERIALS AND METHODS

Patients

Patients with primary distal gastric cancer undergoing TLDG in the Department of Gastrointestinal Surgery, First Hospital of Jilin University between February 2010 and November 2015 were eligible for this study. Inclusion criteria were: (1) distal gastric cancer diagnosed from specimens obtained during pre-operative endoscopic biopsy; (2) endoscopy and computed tomography scan performed to determine pre-treatment tumour site, invasion depth, and the extent of lymph node metastases and metastatic disease and (3) undergoing B-I (delta-shaped) anastomosis or B-II anastomosis. Exclusion criteria were: (1) distant metastases; (2) patients with contraindications to laparotomy or (3) patients who suffered excessive bleeding during TLDG. This study was approved by the Ethics Committee at the First Hospital of Jilin University (JLUFHC1792013), and written informed consent was obtained from all patients before surgery. All procedures were performed by the same experienced laparoscopic surgeon.

Surgical procedure

All patients elected to undergo TLDG. Patients were administered general anaesthesia and were operated in the supine position with the legs apart. A verses needle was used to establish pneumoperitoneum. Subsequently, a 10-mm trocar was placed in the infraumbilical position, a 12-mm and 5-mm trocar were placed in the right upper quadrant and mid abdomen, and two 5-mm trocars were placed in the left upper quadrant and mid abdomen. D2 lymph node dissection was performed in all patients, as recommended by the Japanese Classification of Gastric Carcinoma.[9] Gastrotomy was performed to ensure R0 tumour resection and acceptable tension for anastomosis. Intracorporeally, the specimen was placed in a plastic retrieval bag, small incisions were made at the infraumbilical position, and the resected specimen was removed [Figure 1]. Then, intracorporeal B-I or B-II gastrojejunostomy was performed, depending on the surgeon's preference. B-I anastomosis was mainly applied to patients with carcinoma in the lower third of the gastric body, located ≥2 cm away from the pylorus.

Figure 1

(a) Post-operative wound following totally laparoscopic distal gastrectomy with Billroth I anastomosis. (b) Post-operative wound following totally laparoscopic distal gastrectomy with Billroth II anastomosis

Intracorporeal Billroth-I (delta-shaped) anastomosis using a laparoscopic linear stapler in totally laparoscopic distal gastrectomy

Intracorporeal B-I anastomosis was performed, as previously described.[10] Briefly, a small incision was created on the greater curvature side of the remnant stomach and posterior side of the duodenum. A 60-mm endoscopic linear stapler (ECHELON 60; Ethicon Endo-Surgery, Cincinnati, OH, USA) was inserted, one jaw in each incision, through the left lower quadrant port. The stapler was used to close the posterior wall of the stomach and duodenum. A V-shaped anastomosis was made on the posterior wall and inspected for bleeding. The common stab incision was closed with one 60-mm endoscopic linear staple and the posterior walls were joined[10] [Figure 2].

Figure 2

Billroth I anastomosis: (a) an endoscopic linear stapler was used to create the anastomosis; (b) the common entry hole was closed using the linear stapler; (c) completion of the gastroduodenostomy

Intracorporeal Billroth-II anastomosis using a laparoscopic linear stapler in totally laparoscopic distal gastrectomy

Intracorporeal B-II anastomosis was performed, as previously described.[11] Briefly, a small hole was made 20 cm distal to the ligament of Treitz on the antimesenteric border of the jejunum. The cartridge fork of the 60-mm linear stapler (ECHELON 60; Ethicon Endo-Surgery) was inserted into the tip of the greater curvature side of the remnant stomach, another fork was inserted into the jejunum, and a functional side-to-side antecolic antiperistaltic gastrojejunostomy was created. The anastomosis was inspected for bleeding, and the common enterotomy was closed vertically with a 60-mm linear staple[11] [Figure 3].

Figure 3

Billroth II anastomosis: (a) an endoscopic linear stapler was used to create the anastomosis; (b) the common entry hole was closed using the linear stapler; (c) completion of the gastrojejunostomy

All patients underwent post-operative fluoroscopy before consuming a liquid diet to reveal any leakage or stenosis of the anastomosis [Figure 4].

Figure 4

Post-operative fluoroscopy reveals no leakage or stenosis of the anastomosis: (a) Billroth I anastomosis; (b) Billroth II anastomosis

Data collection

Perioperative data were retrospectively collected from all enrolled patients. Information included age, gender, body mass index (BMI), lymph node dissection, number of stapler cartridges used, time required to create the anastomosis, operative time, estimated blood loss, length of proximal and distal margins and number of lymph nodes harvested. Clinical and pathological staging was performed according to the American Joint Committee on Cancer seventh edition of Gastric Cancer tumour nodes metastasis Staging.[12] Short-term post-operative outcomes evaluated during the initial 30 days after surgery included time to first flatus and earliest liquid consumption, as well as the length of post-operative hospital stay and incidence of post-operative complications.

Statistical analysis

Statistical analyses were performed using SPSS® version 18 software (SPSS Inc., Chicago, IL, USA). Data are expressed as mean ± standard deviation. Means were compared with the independent Student's t- test; categorical data were analysed by Chi-square test. P < 0.05 was considered statistically significant.

RESULTS

A total of 78 patients with primary distal gastric cancer undergoing TLDG with B-I (n = 37) or B-II (n = 41) anastomosis were included in this analysis and followed up. The mean age was 57 years old in the B-I group and 63 years old in the B-II group, with a 1.4:1.0 male-to-female ratio. The demographic and clinical characteristics of these patients are summarised in Table 1. D2 lymphadenectomy was performed in all patients, and there was no conversion to open surgery. Perioperative data are shown in Table 2, and post-operative outcomes and complications associated with TLDG are listed in Tables 3 and 4.

Table 1

Demographic and clinical characteristics of patients

Variable	n (%)		P
	B-I (n=37)	B-II (n=41)
Median age (year)	57 (37–65)	58 (38–70)	0.56
Gender
Male	22	24	0.93
Female	15	17
BMI (kg/m2)	21.83±1.85	21.75±1.42	0.82
ASA score
1	34 (91.89)	36 (87.80)	0.55
2	3 (8.11)	5 (12.20)
3	0	0
Tumour location
Middle third of gastric body	7 (18.91)	28 (68.29)	<0.001
Lower third of gastric body	30 (81.08)	13 (31.71)
Tumour size (cm)	1.91±0.64	2.07±0.67	0.55
Pre-operative haemorrhage	10 (27.02)	14 (34.15)	0.49
Pre-operative haematocrit	0.38±0.06	0.37±0.05	0.29
Pre-operative albumin (g/dl)	36.11±4.22	36.17±4.38	0.36

BMI: Body mass index, ASA: American Society of Anesthesiology, B-I: Billroth I, B-II: Billroth II

Table 2

Surgical outcomes

Variable	B-I (n=37)	B-II (n=41)	P
Number of harvested lymph nodes	24.54±4.66	23.78±5.32	0.15
Number of metastatic lymph nodes	0.38±1.38	0.20±0.64	0.15
Stage
Ia	33	36	0.88
Ib	3	3
II	1	2
≥III	0	0
Resected margin (cm)
Proximal	3.63±1.16	3.36±1.28	0.33
Distal	4.15±1.12	4.59±1.17	0.10
Operative time (min)	153.57±18.25	120.17±11.74	0.004
Anastomosis time (minute)	31.92±6.10	25.29±3.84	0.01
Number of stapler cartridges used	6.68±0.88	6.80±0.78	0.50
Mean EBL (ml)	140.81±29.84	137.68±29.58	0.64
Length of the incision (cm)	2.21±0.33	2.3±0.54	0.54

EBL: Estimated blood loss, B-I: Billroth I, B-II: Billroth II

Table 3

Post-operative outcomes

Variables	B-I (n=37)	B-II (n=41)	P
First flatus (days)	2.59±1.07	2.34±1.38	0.37
Liquid diet (days)	3.38±1.06	3.07±0.84	0.16
Length of hospital stay (days)	10.38±2.78	10.78±2.08	0.47

B-I: Billroth I, B-II: Billroth II

Table 4

Post-operative complications

Variables	B-I (n=37)	B-II group (n=41)	P
Complications
I–II	8	8	0.76
Pulmonary infection	1	1
Celiac infection	1	0
Urinary infection	1	1
Incision infection	1	2
Bile regurgitation	2	3
Ileus	1	1
Gastric atony	1	0
III–IV	0	0

Post-operative complications were graded according to the Clavien-Dindo scoring system. B-I: Billroth I, B-II: Billroth II

Age, gender and BMI were not significantly different between the two groups. There were no significant differences in tumour size, number of harvested and metastatic lymph nodes, stage or distribution of surgical resected margins between the two groups [Table 1]. B-I anastomosis was mainly applied to patients with carcinoma in the lower third of the gastric body (B-I, 81.08% vs. B-II, 31.71%; P < 0.001).

Mean operating (B-I, 153.57 ± 18.25 min vs. B-II, 120.17 ± 11.74 min; P = 0.004) and anastomosis (B-I, 31.92 ± 6.10 min vs. B-II, 25.29 ± 3.84 min; P = 0.01) times were significantly longer for B-I compared to B-II. The number of stapler cartridges used and estimated blood loss did not differ between the two groups [Table 2].

Postoperatively, the time to first flatus and liquid consumption and length of hospital stay were not significantly different between the two groups [Table 3].

There was no anastomotic leakage or bleeding in either group. One patient who underwent B-I anastomosis suffered delayed gastric emptying, as diagnosed by post-operative fluoroscopy. The patient was managed with nasogastric aspiration and total parenteral nutrition. One patient in each group suffered from ileus. However, these patients recovered without the need for surgical management. There were no significant differences in the incidence of complications between groups [Table 4]. Furthermore, there was no mortality during the 30-day follow-up.

DISCUSSION

This study evaluated the practicality, safety and short-term operative outcomes of B-I (delta-shaped) and B-II anastomosis for digestive tract reconstruction in TLDG for gastric cancer. Results revealed a significantly longer operative and anastomosis time for B-I anastomosis compared to B-II anastomosis. However, short-term patient outcomes were similar. In clinical practice, the technique for reconstruction after the surgical resection of gastric cancer is mainly dependent on surgeon preference. More studies are needed to explore the indications for B-I and B-II anastomosis in TLDG for gastric cancer. The data obtained from the present study indicate that both techniques are safe and feasible, although B-I anastomosis may be more time-consuming.

In 1992, Goh et al. first reported on TLDG, describing the use of laparoscopic linear staplers to perform a simple gastrectomy with intracorporeal B-II anastomosis for gastric ulcer.[13] In 2002, Kanaya et al. first reported on the use of LDG with intracorporeal anastomosis (delta-shaped anastomosis) for gastric cancer.[10] Since then, different methods have been developed for TLDG. However, a practical, safe and efficacious reconstruction method remains to be established.

The RY, B-I and B-II approaches are reconstruction methods that are frequently used after distal gastrectomy. The RY procedure forms a tension-free anastomosis, efficiently prevents the reflux of digestive fluids, and is associated with a low incidence of remnant gastritis and anastomotic leakage.[1415] However, the procedure is labour intensive, as it requires two anastomoses, proximal closure of the jejunum and the extensive use of laparoscopic linear staplers. Therefore, it is a long, complex and costly operation.[16171819] Consequently, RY gastrojejunostomy in TLDG is not a preferred option for surgical reconstruction, and this procedure was not investigated as part of the present study.

B-I anastomosis is the optimal reconstruction method after gastrectomy since it is technically simple and maintains the physiological continuity of the intestine. However, B-I reconstruction can be challenging, because a large portion of the stomach is removed, and tension at the site of anastomosis is problematic. In addition, B-I anastomosis for intracorporeal gastroduodenostomy requires precise laparoscopic manipulations, as the tissue around the duodenal stump should be dissected to enable suturing, which may be associated with ischemia and leakage. In the present study, B-I anastomosis was mainly applied to patients with carcinoma in the lower third of the gastric body. Furthermore, the tumour size in patients undergoing B-I anastomosis was smaller compared to those undergoing B-II anastomosis, although the difference was not significant. One patient suffered delayed gastric emptying after B-I anastomosis, which was possibly due to the exaggeration of the anastomosis angle, resulting from adhesions caused by radical removal of the tissue around the duodenum during reconstruction. Based on these observations, we recommend B-I anastomosis for patients with early-stage carcinoma in the lower third of the gastric body.

B-II anastomosis is the most common reconstruction method for patients with tumours localised to the upper gastric body, as it is a simple procedure associated with a low rate of gastric stasis. B-II anastomoses may be constructed with a linear or circular stapler. Compared to the traditional circular stapler, a linear stapler does not require a purse-string suture at the duodenal stump and is especially more convenient in those with a thickened abdominal wall or small abdominal cavity.[6] However, patient outcomes following B-II anastomosis in TLDG have not been fully evaluated. The present study revealed no significant difference in the time to first flatus and liquid consumption or the length of hospital stay in patients who underwent B-I or B-II anastomosis. Furthermore, post-operative short-term outcomes in TLDG were similar to those previously reported for laparoscopy-assisted radical gastrectomy in our institution. Taken together, these findings suggest that TLDG with B-I or B-II anastomosis is an effective procedure in gastric cancer.[20]

There are several limitations associated with the present study. First, TLDG and LDG were not compared. Second, the sample size was small. Finally, the long-term outcomes of B-I or B-II anastomosis in TLDG were not evaluated.

CONCLUSIONS

TLDG with B-I anastomosis or B-II anastomosis is safe and practical for gastric cancer. B-II anastomosis may require less time than B-I anastomosis. More studies are needed to substantiate these findings and further explore the indications for B-I and B-II anastomosis in TLDG for gastric cancer.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.