A comparison of total versus partial omentectomy for advanced gastric cancer in laparoscopic gastrectomy

Laparoscopic gastrectomy for advanced gastric cancer (AGC) is not widely used, but interest in the procedure is increasing [1‐3]. Therefore, in Korea, the KLASS-02 trial (NCT01456598) began in 2012 to compare laparoscopic and open subtotal gastrectomy in local AGC. In the surgical procedure for AGC, D2 dissection with total omentectomy is mandatory for both laparoscopic gastrectomy and open gastrectomy. Although D2 dissection has an oncologic benefit in AGC, the role of total omentectomy is still questionable, particularly for serosa-negative AGC [4, 5]. In fact, dissection through the avascular plane with proper countertraction of the transverse colon can lead to rapid and satisfactory total omentectomy during open surgery; however, in laparoscopic gastrectomy, total omentectomy is time-consuming and poses a risk of injury to the adjacent organs, particularly the spleen and colon. According to the Japanese gastric cancer treatment guidelines, partial omentectomy may be performed in cases of T1 and T2, and total omentectomy is the standard procedure for T3 or deeper tumors [6]. The main purpose of performing total omentectomy is to remove all of the potential seeding lesions in the event of serosal exposure of the tumor cells (T4a). The aim of this study was to elucidate the feasibility of partial omentectomy, based on surgical and oncologic aspects, compared with total omentectomy during laparoscopic gastrectomy for serosa-negative AGC.

Laparoscopic gastrectomy for early gastric cancer (EGC) has been widely performed, and its advantages over open gastrectomy have been verified in many randomized clinical trials [7‐11]. Recently, laparoscopic gastrectomy for AGC has been increasingly performed, and certain reports have outlined its feasibility from technical and oncologic perspectives [1‐3]. In laparoscopic gastrectomy for AGC, D2 dissection and total omentectomy have been the primary troublesome issues for many laparoscopic surgeons.

Although the greater omentum is known to play a role in peritoneal defense by adhering to sites of inflammation and absorbing bacteria and other contaminants, it is a common site of both recurrent disease and primary seeding in gastrointestinal malignancies [12]. Additionally, several experimental studies have reported that cancer cells seeded in the peritoneal cavity preferentially grow on the omentum [12, 13]. For this reason, total omentectomy has been a standard operative procedure during open gastrectomy, regardless of tumor depth. However, if there is no serosal exposure, cancer cell spillage or spread through the omentum is not theoretically possible. Therefore, we hypothesized that partial omentectomy is sufficient for T2 and even T3 cases. The most important type of recurrence relevant to omentectomy may be carcinomatosis. Kim et al. and Ha et al. reported no survival difference between TO and PO in EGC [14, 15]. Kim et al.[16] reported no difference in the pattern of recurrence between TO and PO in AGC without serosal exposure during open gastrectomy. The researchers also detected no difference in the rate of peritoneal metastasis among all recurrences (35% and 25% in TO and PO, respectively). In our series, although more recurrences were noted in the TO group than in the PO group, there was no difference in survival between the two groups. In addition, there was no difference in the occurrence of carcinomatosis between the two groups. Interestingly, approximately half of the T3 cases (25 cases) in the TO group were regarded as including definite serosal invasion (T4a) intra-operatively but were finally proven to encompass subserosal invasion (T3) histologically. Despite the paucity of serosal exposure in the pathologic findings, certain investigators believe that the peritoneum can form a new surface over exposed cancer cells in clinically T4a lesions. Koji et al. reported that the width of subserosal invasion is an independent risk factor for survival in histologically confirmed T3 gastric cancer [17]. We believe that clinical serosal exposure in histologically confirmed T3 cases involves a larger width of subserosal invasion or even focal serosal penetration, which may be why the number of recurrences was much higher in the TO group.

Regarding the high incidence of remnant gastric cancer, we were unable to determine the exact reason because all of the cases had negative margins for malignancy and because remnant gastric cancer lesions were not involved in the anastomosis line. The Japanese gastric cancer treatment guidelines (2010; version 3) recommend leaving a proximal margin of at least 3 cm in the presence of an expansive growth pattern and of 5 cm in the presence of an infiltrative growth pattern or evaluating frozen sections when these factors cannot be observed [6]. Considering that the interval between the initial operation and the completion of gastrectomy was relatively short (1 year for 2 patients and 2 years for the others), there may have been undetected cancer lesions in the remnant stomach, despite preoperative gastrofiberscopy.

Moriguchi et al.[18] have reported that serosal invasion and Borrmann type 4 carcinoma are independent risk factors for the development of carcinomatosis. Although no randomized controlled trials have been performed, Fugita et al.[19] also showed that the type of omentectomy was not a risk factor for recurrence in serosa-negative AGC in a retrospective study, and they included several serosal exposure cases (T4a). The researchers also showed that the development of carcinomatosis has no relationship with the type of omentectomy. The most important factor for justifying the selection of partial omentectomy is tumor depth. The accuracy of preoperative evaluation by endoscopic ultrasonography (EUS) was reported to be 85.7%, and Kim et al. reported that the accuracy of macroscopic findings in determining whether a tumor had invaded the serosa was 87% [16]. Therefore, if we select the type of operation conservatively, with consideration of preoperative evaluations, we can avoid performing partial omentectomy in T4a cases.

In previous reports comparing total omentectomy and partial omentectomy in EGC, partial omentectomy showed several advantages over total omentectomy, including in operation time, perioperative complications, and the postoperative albumin level [14, 15]. Total omentectomy in open gastrectomy is no more difficult than partial omentectomy. With traction of the transverse colon by an assistant, the dissection of the greater omentum can be easily performed through the avascular plane. Otherwise, in laparoscopic gastrectomy, total omentectomy can be a more challenging procedure because maintaining the dissection line through the avascular plane and dividing the omental tissue from the mesocolon are not easy, particularly in patients with a high BMI. In the present study, PO demonstrated several advantages in terms of surgical outcomes. The omentectomy time was shorter, and omentectomy-related complications did not occur in the PO group. However, omental infarction may occur during PO and can appear as carcinomatosis or omental recurrence in radiologic findings [3]. It is important to differentiate between various radiological findings and omental infarcts [20], and close follow-up is required when differentiation is difficult, particularly in the immediate postoperative period.

Because the present study was retrospectively designed, it has certain limitations. Although there was no significant difference in the distribution of stages between the two groups, the TO group contained more advanced cases. These discrepancies in tumor staging may influence the recurrence rate. However, omentectomy was not risk factor for recurrence in the multivariate analysis. Despite these limitations, the present study is valuable because previous reports were based on open gastrectomy, so this is the first report to evaluate the role of the type of omentectomy in laparoscopic gastrectomy for serosa-negative AGC.

In conclusion, partial omentectomy can be a useful alternative method for performing laparoscopic gastrectomy for serosa-negative AGC. However, to determine long-term technical and oncologic safety, a prospective randomized controlled trial is needed.