Comparison of laparoscopy-assisted and totally laparoscopic Billroth-II distal gastrectomy for gastric cancer

Since the first performance by Kitano et al. [1], the use of laparoscopy-assisted distal gastrectomy (LADG) for early gastric cancer (EGC) in Korea and Japan has exploded because of the high prevalence of EGC and the merits of LADG, including less post-operative pain, earlier recovery and better cosmetic outcomes, over open gastrectomy [2-4]. Following laparoscopic distal gastrectomy (LDG), there are three major reconstructive methods, the Billroth-I, Billroth-II and Roux-en-Y, that can be used, and several studies have reported their safety and efficacy [5-7]. In Korea and Japan, Billroth-I is the most common reconstructive modality because of the maintenance of the physiological passage of food. Roux-en-Y reconstruction, which has a low incidence for bile reflux, has also been employed by some centers [5, 7-10]. However, these reconstructive modalities have some problems, such as bile reflux, food stasis and complexity [11-13]. For this reason, Billroth-II reconstruction has commonly been performed after LDG because of its simplicity and the low rate of gastric stasis [13]. Although laparoscopy provides a wider surgical field than mini-laparotomy, in general, most surgeons have chosen mini-laparotomy at the upper abdomen for reconstruction because of the technical complexity of LDG and an unfamiliarity with intra-corporeal anastomosis. As surgeon experience in performing LDG has increased and improvements in laparoscopic instruments have been accomplished, for example, the development of the endoscopic linear stapler, totally laparoscopic distal gastrectomy (TLDG), including several intra-corporeal anastomotic techniques, has been introduced and its usefulness reported [5, 9, 14, 15]. However, these reports have been mainly restricted to the Billroth-I and Roux-en-Y for reconstruction. In this study, we evaluated the safety and short-term outcomes of TLDG with reverse T-shaped intra-corporeal Billroth-II anastomosis using linear staplers.

The major difference between LDG and conventional open distal gastrectomy is the length of the incision on the abdomen. Because of the smaller incision, LDG has advantages over open distal gastrectomy, such as early recovery with a less painful post-operative course and cosmetic efficacy. Most surgeons perform LADG, which consists of an appropriate systemic lymph node dissection and the mobilization of the stomach. LADG makes an approximately 5- to 6-cm long mini-laparotomy on the upper abdomen to perform extra-corporeal reconstruction. This reconstructive modality might lead to pain and increased injury from the forceful traction at the mini-laparotomy site. In our result, additional analgesics were required more frequently in the LADG group. In addition, extra-corporeal reconstruction via mini-laparotomy might be a complicated, stressful and time-consuming procedure. During extra-corporeal reconstruction, we performed hand-sewed anastomosis; however, extraction of the gastric remnant and jejunum via a narrow window was not easy and did not supply sufficient exposure of the lumens, especially in obese patients. We usually had a time restriction because the greater the length of time taken for an anastomosis, the greater the potential for congestion in the gastric remnant and jejunum, which might lead to anastomotic leakage. In contrast to the extra-corporeal procedure, intra-corporeal reconstruction offers a wider operative field than minilaparotomy and requires a shorter time because it is completed by the firing of the endoscopic linear staplers twice. In this study, the mean time for operation and anastomosis was significantly shorter than in the LADG group.

Our intra-corporeal Billroth-II reconstruction had some differences from conventional Billroth-II reconstruction, which was made between the end of the remnant stomach and the side of the jejunum. Anastomosis in intra-corporeal reconstruction was made at the posterior wall of the remnant stomach parallel to the greater curvature. The merits of this method were as follows. First, it was easy and safe to close the entry hole. During the enveloping of the entry hole, surgeons have generally positioned the endoscopic linear stapler vertical to the direction of the jejunum to prevent potential afferent loop narrowing or obstruction in the proximal jejunal limb. However, it was difficult to perform a vertical closure because of the difficulty in positioning the endoscopic linear stapler. In our procedure, the stapling line for closing the entry hole was oblique to the direction of the jejunum. Although this closure might have potential for afferent loop obstruction, no afferent loop obstruction or related symptoms were observed. One afferent loop obstruction was due to an internal herniation of the entire jejunal segment through the posterior space of the remnant stomach (Petersen hernia). Therefore, this modality was feasible and safe. Second, this procedure reduces the number of trocars. Generally, 5 to 6 trocars, including one or two 12-mm sizes, are used for the operation, and reconstruction is performed at either the right or left side of the patient. However, we used 4 trocars, and the reconstructive procedure was achieved on the right side of the patient without a change in the surgeon's position. This might also be related to the low dose of additional analgesics and the shorter post-operative stay in the TLDG group. Third, it was easy to examine and control the existence of bleeding from the anastomosis site. Bleeding from the stapled line occurred, and in this case, it was necessary to control it. If the entry side was located on the left side of the patient, it was hard to check the stapled line due to the limitation of the direction of the laparoscope.

There were no differences in anastomosis-related morbidities between groups. However, bleeding from the anastomosis site in the intra-corporeal procedure tended to be higher than the extra-corporeal method. With the endoscopic linear stapling device, immediate or delayed bleeding at the stapled line might occur, especially at the anastomosis site between the remnant stomach and jejunum. Four patients actually developed bleeding in the TLDG group in the earlier series. After this series, we examined the presence of bleeding focus by washing with normal saline, and we controlled bleeding with laparoscopic clips to prevent post-operative intra-luminal bleeding. There was one leakage from gastrojejunostomy in the intra-corporeal procedure, which was managed by percutaneous drainage. This rate was acceptable compared with other reports in with intra-corporeal and extra-corporeal reconstructions [13, 17, 18].

Although Billroth-I reconstruction was the typical choice after distal gastrectomy in Korea and Japan because of the preservation of the physiological passage and simple closure using staplers, about 40% of Korean surgeons performed Billroth-II reconstruction [19]. The merits of Billroth-II reconstruction compared to Billroth-I are a lower food stasis rate and a larger extent of resection. If the tumor is located in the middle third of the stomach, it is difficult to perform Billroth I reconstruction because excessive tension might develop at the anastomosis site if a safety margin was included. For this condition, Roux-en-Y reconstruction is recommended as an alternative method [7-10]. The advantages of Roux-en-Y reconstruction are low bile reflux and prevention of bile reflux, thus preventing gastritis and gastric cancer in the remnant stomach [7, 20]. However, this procedure requires multiple anastomosis and involves a risk of Roux stasis. For food stasis, this procedure is stressful to both patients and surgeons, and most Korean surgeons have been reluctant to perform this procedure [6, 19].

An accurate localization of the lesion and confirmation of the tumor-free margin are mandatory for oncological demand. The main concern for intra-corporeal anastomosis is how to determine the resection line for a sufficient proximal margin. During the extra-corporeal procedure, it was not difficult to confirm the resection line because it was possible to palpate the tumor or the clips that had been applied preoperatively. In the intra-corporeal procedure, although the preoperative endoscopic clipping was performed around the lesion, there was little tactile sensation for the lesion, and it was hard to confirm the resection line, especially for a tumor that was located at the middle part of the stomach. For this reason, various methods, such as endoscopic tattooing, intraoperative endoscopy, laparoscopic ultrasonographic localization and intraoperative fluoroscopy, have been introduced to localize the tumor [21-24]. We usually performed an intraoperative portable abdominal radiograph if EGC was located in the middle part of the stomach and a sufficient tumor-free proximal resection margin could be achieved. In the present study, there was no difference in the proximal resection margin.

In conclusion, our results demonstrated that intra-corporeal Billroth-II anastomosis is a feasible procedure that can be safely performed with the proper experience for LDG. This procedure may be less time consuming and may produce a more cosmetic result. However, surgeons should pay attention to prevent bleeding from the staple line, especially when performing intra-corporeal anastomosis using endoscopic linear staples. This study was retrospective and TLDG procedure was performed after many experiences in LADG. Therefore, there was a little limitation for comparing with absolute numerical value between two groups. Therefore, prospective study might be needed to confirm the feasibility and merits of TLDG.