Laparoscopic Completion Total Gastrectomy as a Standardized Procedure for Gastric Stump Cancer: A Case Control Study

We performed a database search and identified 40 patients who had undergone surgery for GSC at Ishikawa Prefectural Central Hospital in Japan from January 2010 to December 2018. One patient who underwent bypass surgery, 1 patient who underwent staging laparoscopy, and 1 patient who underwent robot-assisted completion total gastrectomy were excluded from this study. The remaining 37 patients underwent gastrectomy for GSC and were further classified into 2 groups according to the initial approach of the operation: the LCTG group (n = 17) and the OCTG group (n = 20). The mean ages of patients in the LCTG and OCTG groups were 71.9 ± 8.1 and 68.9 ± 9.1 years, respectively. The male-to-female ratios in the LCTG and OCTG groups were 12 to 5 and 16 to 4, respectively. The medical records of all patients were retrospectively evaluated to compare the short-term surgical and oncological outcomes. The patient characteristics are shown in Table 1.

The use of LCTG for GSC was introduced to our institution in 2010. The exclusion criteria for LCTG are remarkable direct tumor invasion to other organs and patient conditions that preclude laparoscopy. The selection criteria for patients to undergo a laparoscopic or open procedure depends on the degree of tumor progression; invasiveness of the previous operation, which includes the extent of lymph node dissection or inflammatory reaction; and patient preference is equally considered.

A 5-port surgical approach was used. The first 12-mm trocar was inserted at the umbilical area using the Hassan method. The other trocars were subsequently inserted carefully under laparoscopic viewing as in conventional laparoscopy.²²  A 10-mm, 30-degree oblique viewing laparoscope was used, and the CO₂ pressure was maintained at 10 to 12 mm Hg. The Harmonic Scalpel (Ethicon EndoSurgery Inc., Cincinnati, OH), which is an ultrasonic-activated device, and the LigaSure (Medtronic, Minneapolis, MN) were used for adhesiolysis and radical lymphadenectomy. The extent of lymph node dissection was based on the recommendations for total gastrectomy from the Japanese gastric cancer treatment guidelines.²³  In cases of benign disease at the initial surgery, the intact gastric vessels were dissected from the root, and the resected specimen was extracted through the umbilical incision, which was enlarged to the minimum size required for extraction.

The gastrosplenic ligament was resected, starting with the opening of the omental bursa, and adhesions between the posterior gastric wall and pancreas were carefully divided. The dissection was carefully performed because the inferior surface of the left lateral segment of the liver was often severely adhesive to the remnant gastric wall. Moreover, the pneumoperitoneum yielded bloodless dissection. After encirclement of the gastro-duodenal anastomosis, the duodenum was transected using a linear stapler. Subsequently, the remaining dissection around the remnant stomach including the vessels was completed, and the lower esophagus was transected in the same manner.

The afferent and efferent loops of the jejunum or Roux limb were resected, securing sufficient distance from the anastomosis. The mesenteric lymph nodes were dissected depending on the tumor size or invasion.

Reconstruction after the complete removal of the GSC was performed with the Roux-en-Y method. The jejunum was transected 25 cm from the ligament of Treitz. Approximately 20 cm of the jejunum on the anal side was sacrificed, and the Roux limb was prepared. Jejunojejunostomy was performed with the Y limb. The Roux limb was ascended through the antecolic route, and esophagojejunostomy was performed using the linear stapler. The mesenteric gap at the Y limb and Petersen's mesenteric defect were closed by continuous suturing using barbed strings.

Patient ages are presented as mean ± SD, and all other values are expressed as median with range. All statistical analyses were completed using R statistical software, version 3.5.0 (R Foundation for Statistical Computing, Vienna, Austria). Chi-squared, Fisher's exact, and Mann–Whitney U tests were performed to compare the 2 groups, and values of P < 0.05 were considered statistically significant.

No significant differences in sex distribution, body mass index, and comorbidity incidence were observed between the 2 groups (Table 1). A total of 5 and 12 initial gastrectomies were performed in the LCTG group for benign and malignant diseases, respectively. In contrast, a total of 4 and 16 initial gastrectomies were performed in the OCTG group for benign and malignant diseases, respectively. However, the difference observed between the groups was not statistically significant. The median time from the initial gastrectomy to the development of GSC was comparable between the LCTG and OCTG groups (11 versus 15.5 years, respectively; P = 0.385). The most common tumor location in the LCTG and OCTG groups was the nonanastomotic site (12 [70.6%] and 14 [70%] cases, respectively). However, only 3 cases in each group had the tumor detected at the anastomotic site (17.6% and 15% in the LCTG and OCTG groups, respectively).

Two (11.8%) and 7 (35.0%) patients in the LCTG and OCTG groups, respectively, were diagnosed with tumor depth invasion greater than clinical T stage 3. However, no significant difference in the distribution of the clinical T stage was observed between the groups. No patients in the LCTG group had preoperative lymph node metastasis. Therefore, patients in the LCTG group, except for those with clinical T stage 3, were considered to be at clinical stage I. The clinical stages in the OCTG group were diversely distributed; however, no significant difference in the stage distribution was observed between the groups. In the initial gastrectomy, 6 (35.3%) and 3 (15.0%) patients in the LCTG and OCTG groups, respectively, were treated with laparoscopy; however, no significant difference in the frequency of laparoscopy was observed between the groups. The type and reconstruction of the initial gastrectomies were diverse; however, no significant difference in the distributions was observed for both groups. The most common reconstruction method in the initial gastrectomy was Billroth I anastomosis in 7 (41.2%) and 8 (40.0%) patients in the LCTG and OCTG groups, respectively.

The surgical outcomes are depicted in Table 2. The median operation times were 230 (140–400) minutes and 182.5 (130–360) minutes in the LCTG and OCTG groups, respectively, representing a significant difference (P = 0.026). The median estimated blood loss was significantly different between the 2 groups: 14 (4–100) mL in the LCTG group and 105 (5–840) mL in the OCTG group (P < 0.001). Although no significant difference in the extent of lymphadenectomy and morbidity was observed between the 2 groups, 2 patients in the OCTG group had major complications (Clavien-Dindo classification > grade IIIa). No conversion to open surgery was reported in the LCTG group. The median time to first flatus passage was significantly shorter in the LCTG group than in the OCTG group (2 versus 3 days; P < 0.001). No significant difference in analgesic usage after postoperative day 5 (0 versus 1 time; P = 0.334) or in the duration of postoperative hospitalization (13 versus 14 days; P = 0.657) was observed between the 2 groups.

The pathologic findings of the resected specimens are shown in Table 3. The median tumor size in the LCTG group was significantly smaller than that in the OCTG group (26 versus 40 mm; P = 0.0457). No significant difference in the median number of retrieved lymph nodes (11 versus 9.5; P = 0.437), depth of the tumor invasion (P = 0.12), extent of lymphatic metastasis (P = 0.0509), distant metastasis ratio (P = 1), and variation of histological type (P = 1) were observed between the 2 groups. However, the median number of metastatic lymph nodes in the LCTG group was significantly lower than that in the OCTG group (0 versus 0.5; P = 0.0108). In addition, the pathologic stage distribution in the LCTG group was lower than that in the OCTG group (P = 0.0346).

Our results confirm the feasibility of LCTG for the treatment of GSC. Patients in the LCTG group had significantly longer operation times but significantly less blood loss and earlier flatus passage than the OCTG group. Furthermore, no conversion to open surgery and no higher morbidity than Clavien-Dindo class III were reported in the LCTG group.

Yamada et al²⁴ first presented a case report for laparoscopy-assisted resection of gastric remnant cancer in 2005; many additional studies reported successful applications of the technique.^25–33  Therefore, we searched reports of LCTG for GSC from the PubMed database in English literature and summarized the data by case reports (Table 4) and comparative studies (Table 5). Many surgeons have successfully applied LCTG, and this technique is considered the preferred treatment option (Table 4).^24–33  As shown in Table 5, our results are consistent with those of comparative studies.^14–21 

The patients in the LCTG group had smaller tumor size, lower numbers of metastatic lymph nodes, and lower pathologic stages than patients in the OCTG group; however, the clinical stage distribution, dissection, and retrieved lymph nodes showed no significant differences between the groups. In addition, the number of retrieved lymph nodes was equal to that reported in other studies (Table 5).^14–21  The feasibility and validity of LCTG with the strict postoperative surveillance for PGC can increase the number of lower stages of GSC and improve patient survival.⁷ 

The most difficult aspect of the operative procedure for GSC is the adhesiolysis, which is the key factor to safely performing LCTG.¹⁸  A precise and sharp dissection between the adjacent organ and remnant stomach is necessary to avoid organ injury, and less bowel manipulation leads to early recovery.^15,18  We consider laparoscopy an effective solution to overcome this difficulty in the treatment of GSC. The advantages of laparoscopic surgery are pneumoperitoneum, which widens the dissectible layer between the adhered organs, and a magnified view that enables detection of the loose and dissectible layer. Moreover, progressive high definition imaging significantly contributes to the benefits from such magnified views. We have been using the high definition scope system (Karl Storz SE & Co. KG, Tuttlingen, DE) since the introduction of LCTG in our institution. Advanced energy devices and forceps also contribute to refining the quality of surgery, reducing bleeding, reducing the trauma to organs, and refining the precision of lymphadenectomy. Our sophisticated dissection techniques combined with these advanced developments enable us to perform LCTG with an extremely reduced blood loss compared with previous case-controlled studies (Table 5), leading to the earlier recovery of digestive peristalsis.

Robotic gastrectomy could be a future advancement for the treatment of GSC in terms of its visual improvement in the surgical field, which is referred to as robotically enhanced surgical anatomy.³⁴  The refined anatomic view of robotic gastrectomy could achieve precise movement of forceps without hand tremors, which could increase operative accuracy. In fact, robotic gastrectomy for PGC has decreased the complication rate despite longer operative time and higher cost than laparoscopic gastrectomy.^35,36  Robotic surgery has already been applied to GSC and reviewed retrospectively, which has shown a lower conversion rate and comparative short-term outcomes to LCTG.³⁷  Similarly, we have been introducing robotic surgery to GSC, and we expect superior results.

We acknowledge some limitations in our study. First, this study had a retrospective design, which could have led to potential selection biases due to surgeon or patient preference. Therefore, a randomized controlled study should be performed. Second, because of the low incidence of GSC, the sample size was too small to elucidate the universal results and superiority of LCTG over OCTG for GSC. Although the incidence of GSC in our institution was 40 cases (3.5%) from 2010 to 2018, this frequency is similar to previously reported ones^2–6 ; therefore, a multicenter study is desired to validate our results.

LCTG for the treatment of GSC was safely conducted with fewer complications and mortalities than previously reported studies. Advanced technologies and sophistication of laparoscopic skills may further yield minimal invasiveness with better short-term outcomes.

We thank Editage (www.editage.com) for English language editing. The authors declare no conflicts of interest and the authors have no financial ties to disclose.

All procedures performed in this study that involved human participants were in accordance with the ethical standards of the institutional and/or national research committee and the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was reviewed and approved by the Ethics Committee of Ishikawa Prefectural Central Hospital. Reference number: 1438. Informed consent was obtained from all individual participants included in the study.