Laparoscopic Radical Gastrectomy for Remnant Gastric Cancer

Remnant gastric cancer (RGC) refers to a primary malignancy developing in the residual stomach after partial gastrectomy, which typically manifests more than five years after surgery. Although RGC has a relatively low incidence (about 2.6%)¹, it is frequently diagnosed at an advanced stage due to its long latency and nonspecific clinical presentation, leading to a poor prognosis². The pathogenesis of RGC is linked to multiple factors, including impaired mucosal defense, bile reflux, chronic inflammation, reconstruction technique, and Helicobacter pylori infection^3,4,5.

Similar to common gastric cancer, the treatment plan for residual gastric cancer mainly depends on the TNM staging. R0 resection is the preferred treatment option, and for patients who can undergo R0 resection, their prognosis is also similar to that of common gastric cancer.

Similar to common gastric cancer, the treatment for RGC mainly depends on the TNM stage. R0 resection is the preferred option, and for patients who can undergo R0 resection, the prognosis is similar to that of common gastric cancer^6,7,8. Although systemic chemotherapy, targeted therapy, and immunotherapy have shown progress in recent years, radical surgery remains the cornerstone of RGC treatment⁹. Conventional open surgery is often not preferred in elderly or high-risk patients due to extensive surgical trauma, high bleeding risk, and a high incidence of postoperative complications. Laparoscopy-assisted surgery for RGC was first reported by Yamada et al. in 2005¹⁰. Since then, with the growing adoption of minimally invasive techniques in gastric surgery, reports on laparoscopic radical gastrectomy (LRG) for RGC have gradually emerged. LRG offers advantages such as minimal trauma, faster recovery, and lower complication rates, making it a promising and increasingly utilized approach for RGC. Multiple studies have confirmed that, in experienced centers, LRG achieves R0 resection rates and lymph node yields comparable to those of open surgery, while significantly reducing intraoperative blood loss, shortening hospital stays, and facilitating faster gastrointestinal recovery^11,12,13.

However, LRG requires excellent anatomical orientation and advanced laparoscopic skills, particularly when dealing with adhesions near the anastomosis, jejunal mesentery, and splenic hilum, where procedural risks are high¹⁴. This article aims to systematically summarize the essential operative techniques and strategies in this procedure.

The protocol was approved by the Institutional Review Board of The First Affiliated Hospital of Jinan University. This study included five patients who underwent LRG for RGC from January 2013 to December 2021.. Written informed consents were obtained from all the patients. The materials and the equipment used are listed in the Table of Materials.

1. Inclusion criteria

1. Include patients with a history of distal gastrectomy for benign or malignant conditions and a diagnosis of RGC more than 5 years after the initial surgery.
2. Confirm that pathological or imaging studies show the tumor is confined to the remnant stomach with no evidence of distant metastasis, and ensure preoperative evaluation confirms operability.
3. Verify through upper gastroenterography, enhanced CT scan, or endoscopy that there is no significant anastomotic stricture or esophageal invasion, indicating the tumor is resectable.

2. Exclusion criteria

1. Exclude patients with unresectable conditions, including peritoneal or liver metastases, or multiple fixed lymph node conglomerates.
2. Exclude patients with severe adhesions from previous upper abdominal surgeries that preclude safe laparoscopic access.
3. Exclude patients with clinically significant cardiac, pulmonary, or renal dysfunction.
4. Exclude patients who cannot tolerate general anesthesia or pneumoperitoneum.

3. Preoperative preparation

1. Perform routine laboratory tests, including complete blood count, urinalysis, stool examination, liver and renal function tests, coagulation function test, and tumor marker analysis.
2. Perform electrocardiography, chest CT, contrast-enhanced abdominal CT (Figure 1A,B), and upper gastrointestinal contrast (Figure 1C) before surgery.
3. Perform endoscopic biopsy to confirm the pathological diagnosis and assess anastomotic patency and tumor extent (Figure 1D).

4. Surgical technique

1. Anesthesia and positioning
   1. Administer general anesthesia via endotracheal intubation (following institutionally approved protocols). Place the patient in a supine position with legs spread at 45°-60°. Disinfect the surgical site using povidone-iodine.
   2. Stand between the patient's legs, with the assistant on the left and the laparoscope holder on the right. Adjust the surgical position intraoperatively as needed. When dissecting areas adjacent to the lateral abdomen, especially if instrument interference occurs with the laparoscope, stand on either side of the patient while the laparoscope holder moves between the patient's legs.
2. Pneumoperitoneum establishment and port placement
   1. Make a 10 mm vertical infraumbilical incision for Veress needle insertion and establish pneumoperitoneum by CO₂ insufflation to a pressure of 12 mmHg.
   2. Insert a 10 mm trocar at the umbilical site for laparoscope introduction. Under direct visualization, place two 12 mm trocars in the bilateral mid-abdomen and two 5 mm trocars in the bilateral upper abdomen.
3. Intraoperative exploration and adhesiolysis
   1. Conduct a thorough assessment of adhesions within the abdominal cavity and evaluate the presence of tumor implantation and infiltration of adjacent organs (Figure 2A-D). To avoid injury to the jejunal limb, pancreatic tail, mesocolon, and portal vein trunk, perform adhesiolysis using a combination of blunt and sharp dissection (Figure 2E,F).
      NOTE: Pay attention to areas prone to adhesions, such as the left hepatic lobe and remnant stomach, the transverse colon and greater omentum, and the splenic hilum and pancreatic tail.
4. Lymphadenectomy and organ mobilization
   1. Tailor lymphadenectomy for RGC according to the prior surgical approach, tumor location, and initial reconstruction method (Billroth I/II/Roux-en-Y). Follow the standard D2+ radical surgery guidelines, with special attention to ectopic nodes around the celiac axis, splenic hilum, and jejunal mesentery (Figure 3A-F, Figure 4A-F).
      NOTE: During lymph node dissection, maintain awareness of altered lymphatic drainage pathways resulting from previous gastric surgery. Pay particular attention to ectopic lymph nodes located along the mesenteric border and adjacent to the colic arteries to avoid missed metastases.
   2. Mobilize the cardia and at least 6 cm of the distal esophagus using an ultrasonic scalpel (Figure 5A) to ensure a safe and tension-free anastomosis, especially for tumors involving the cardia or distal esophagus.
      NOTE: If the lesion involves the pancreatic tail or splenic hilum, perform a combined distal pancreatectomy or splenectomy as indicated.
5. Remnant stomach resection and digestive tract reconstruction (Roux-en-Y anastomosis)
   1. For cases with previous distal gastrectomy and Billroth II reconstruction, transect the jejunal input and output loops at the prior gastrojejunostomy using a linear stapler (Figure 5B,C).
      NOTE: If the tumor involves the previous gastrojejunostomy, remove the jejunal input and output loops approximately 10 cm away from the anastomosis.
   2. When the tumor does not involve the cardia, perform a side-to-side esophagojejunostomy using a linear stapler before transecting the lower esophagus to prevent retraction into the thoracic cavity after transection (Figure 5D-F).
      NOTE: When the tumor involves the cardia, first transect the lower esophagus using a linear stapler to preserve tumor integrity, then perform side-to-side esophagojejunostomy.
   3. Perform a side-to-side jejunojejunostomy at the distal jejunum located 45 cm from the esophagoduodenal anastomosis (Figure 6A,B).
      NOTE: Ensure all anastomoses are tension-free and patent to prevent leakage and stenosis. Inject the methylene blue solution through the gastric tube after completion of all anastomoses. Absence of dye leakage confirms anastomotic integrity.
6. Specimen extraction and incision suturing
   1. Place the resected specimen in a sterile retrieval bag. Irrigate the surgical field with sterile distilled water to ensure hemostasis and confirm the absence of gastric leakage (Figure 6C).
   2. Place one or two drainage tubes near the left subphrenic space and around the jejunal anastomosis to facilitate postoperative monitoring and prevent complications such as anastomotic leakage (Figure 6C).
   3. Extend the umbilical incision to approximately 6-8 cm to remove the specimen bag. Send the sample for intraoperative rapid frozen pathological examination and postoperative routine pathological analysis (Figure 6D). After confirming negative margins via frozen section, remove all trocars and close the abdominal incisions to complete the procedure.

5. Postoperative procedure

1. Continuously monitor vital signs, including heart rate, blood pressure, respiratory rate, and temperature, to enable early detection and management of postoperative complications.
2. Administer intravenous antibiotics, somatostatin analogs, and hepatoprotective agents, and adjust regimens based on individual patient conditions. For patients without infectious complications, ensure that prophylactic antibiotic use after surgery does not exceed 48 h.
3. Inspect surgical incisions regularly for signs of infection, such as erythema or exudate, and provide prompt intervention when infection is suspected.
4. In the absence of anastomotic leakage, remove abdominal drains 5-7 days after surgery.
5. Perform routine blood tests regularly, including complete blood count and other relevant parameters.

A total of 5 patients (median age: 73 years, range: 57-77 years), all of whom were male, underwent laparoscopic radical gastrectomy for remnant gastric cancer. The original disease in all cases was benign, and all patients had previously undergone open distal gastrectomy with Billroth-II reconstruction. The median interval between the initial surgery and the diagnosis of remnant gastric cancer was 480 months (range: 300-696 months). The median body mass index (BMI) of the patients was 22.1 kg/m2 (range: 20.1-26.6 kg/m2). Preoperative laboratory findings showed a median white blood cell count of 7.16 × 109/L (range: 2.21-9.81 × 109/L), hemoglobin level of 105 g/L (range: 74-115 g/L), and platelet count of 230 × 109/L (range: 62-488 × 109/L). The median serum carcinoembryonic antigen (CEA) level was 1.64 ng/mL (range: 0.73-14.66 ng/mL) (Table 1).

All patients successfully underwent LRG without conversion to open surgery. The median operative time was 380 min(range: 264-660 min), and the median intraoperative blood loss was 100 mL(range: 100-300 mL). No intraoperative complications occurred in any of the five patients (0.0%). The median postoperative drainage duration was 6 days(range: 4-9 days), and the median time to first defecation was 4 days(range: 2-6 days). The median postoperative hospital stay was 11 days(range: 8-22 days). One patient developed a pulmonary infection, while no cases of incision infection, abdominal infection, postoperative bleeding, ascites, or anastomotic leakage were observed. The patient who developed a postoperative pulmonary infection mainly presented with a temperature exceeding 39 °C, and was treated with sensitive antibiotics until the temperature returned to normal for 72 h. Regarding pathological findings, the pathological T classification was T3 in 3 patients and T4 in 2 patients. Pathologic N classification showed that 2 patients had no lymph node metastasis (N0), while 3 patients had positive lymph node involvement, including N1 in 1 patient and N3 in 2 patients. All patients were classified as pM0, with no evidence of distant metastasis. Histologically, 3 cases were moderately differentiated, and 2 cases were poorly differentiated (Table 2).

Figure 1: Preoperative examination. (A) The cross-sectional CT scan indicated a mass at the gastrojejunostomy site. (B) The coronal CT scan indicated a mass at the gastrojejunostomy anastomosis. (C) Upper gastrointestinal contrast examination revealed an area of filling defect at the anastomosis site of the Billroth-II gastroduodenostomy. (D) Gastroscopy revealed a mass with an ulcer at the gastrojejunostomy anastomosis. Please click here to view a larger version of this figure.

Figure 2: Intraoperative exploration and adhesiolysis. (A) Exploration of the left upper abdomen. (B) Exploration of the right upper abdomen. (C) Exploration of the lower abdomen and the pelvic region. (D) Adhesion between the omentum and the abdominal wall. (E) Adhesions around the gastrojejunostomy anastomosis. (F) Separate and release the adhesions around the gastrojejunostomy anastomosis. Please click here to view a larger version of this figure.

Figure 3: Lymphadenectomy (Part 1). (A) Lymph node dissection of the greater curvature of the stomach (No.4). (B) Lymph node dissection of the celiac trunk (No.9). (C) Lymph node dissection of the common hepatic artery (No.8). (D) Lymph node dissection of the left gastric artery (No.7). (E) Lymph node dissection of the ligamentum hepatoduodenale (No.12a). (F) Completion of the regional lymph node dissection at the D2 station. Please click here to view a larger version of this figure.

Figure 4: Lymphadenectomy (Part 2). (A) Lymph node dissection of the proximal splenic artery (No.11p). (B) Lymph node dissection of the distal splenic artery (No.11d). (C) Lymph node dissection of the splenic hilar (No.10). (D) Lymph node dissection of the lesser curvature of the stomach (No.3). (E) Lymph node dissection of the right cardia (No.1). (F) Lymph node dissection of the left cardia (No.2). Please click here to view a larger version of this figure.

Figure 5: Remnant stomach resection and esophagojejunostomy. (A) Mobilization of at least 6 cm of the distal esophagus. (B) Transection of the jejunal input loop at the previous gastrojejunostomy site. (C) Transection of the jejunal output loop at the previous gastrojejunostomy site. (D) Side-to-side esophagojejunostomy. (E) Transection of the lower segment of the esophagus. (F) Closure of the esophagojejunal anastomotic gap with sutures. Please click here to view a larger version of this figure.

Figure 6: Jejunojejunostomy and resected specimen. (A) Side-to-side jejunojejunostomy.(B) Closure of the jejunojejunal anastomotic gap with sutures. (C) Placement of the resected specimen into a sterile retrieval bag and insertion of a drainage tube near the left subphrenic space. (D) Resected remnant stomach specimen. Please click here to view a larger version of this figure.

Table 1: Clinical features of the patients. BMI = body mass index; WBC = white blood cell; HGB = hemoglobin; PLT = platelet; CEA = carcinoembryonic antigen.

Table 2: Surgical outcomes of the patients.

RGC is a primary malignancy that arises in the residual stomach after partial gastrectomy. It was first described by Balfour in 1922¹⁵. Although the overall incidence of RGC remains relatively low, it has been steadily rising due to improvements in gastric cancer detection and increased postoperative survival¹⁶. A previous gastrectomy often results in extensive intra-abdominal adhesions and altered anatomy around the remnant stomach, particularly in lymphatic drainage pathways, thereby significantly increasing the complexity of surgical procedures^17,18. Consequently, surgical success depends heavily on the technical proficiency of the surgeon and effective multidisciplinary collaboration.

In recent years, advancements in laparoscopic techniques and surgical instrumentation have enabled LRG to achieve a safety profile comparable to that of conventional open surgery^19,20,21. The incidence of postoperative complications, including serious events such as anastomotic leakage and pancreatic fistula, does not differ significantly between the two approaches^22,23. Laparoscopic surgery provides several advantages, including reduced operative trauma, lower intraoperative blood loss, faster postoperative recovery, and shorter hospital stays^24,25,26. Importantly, oncologic outcomes such as 3-year disease-free survival and overall survival rates are also comparable between laparoscopic and open approaches^24,25,26. Additionally, the number of harvested lymph nodes and the negative margin (R0) rate achieved in laparoscopic procedures are not inferior²⁷. Therefore, for experienced surgeons, LRG can offer equivalent oncologic efficacy while delivering superior perioperative comfort and expedited recovery. These benefits are largely attributed to minimal tissue disruption, reduced postoperative pain, and the enhanced precision afforded by high-definition magnified visualization during laparoscopic surgery²⁸. This article integrates findings from multiple domestic and international studies to provide a detailed description of the technical aspects of LRG for RGC.

In this study, we enrolled patients with a history of distal gastrectomy who were newly diagnosed with RGC, all of whom had a favorable general health status and no contraindications to anesthesia, thus meeting the indications for laparoscopic radical surgery. However, the feasibility of laparoscopic surgery in patients with advanced-stage disease complicated by extensive adhesions or multi-organ invasion remains controversial. Surgical candidacy in such cases requires a comprehensive assessment that incorporates the surgeon's experience, the capabilities of the surgical center, and individualized risk evaluation. Further prospective studies are necessary to establish robust, evidence-based recommendations for this subgroup of patients.

Intraoperative adhesiolysis remains one of the most technically demanding aspects of RGC surgery, as adhesions are frequently dense and located in critical areas such as between the left hepatic lobe and the gastric remnant, the transverse colon and greater omentum, as well as around the splenic hilum and pancreatic tail. These adhesions often obscure normal anatomical planes and increase the risk of injuring adjacent structures, including the jejunal limb, pancreatic tail, and major vessels. To address this intraoperative challenge, based on our own experiences and relevant literature reports, we recommend a safe approach that involves initiating dissection from non-adherent zones and proceeding gradually into densely adherent regions, with careful use of vascular and neural landmarks to guide the identification of correct tissue planes and minimize inadvertent organ injury²⁹.

In RGC, lymphadenectomy should be individualized based on tumor location and prior reconstruction. The altered lymphatic drainage following previous gastrectomy may result in metastasis to non-standard nodal stations. According to the Japanese Gastric Cancer Association (JGCA) 2021 treatment guidelines, splenic hilar lymph node dissection with splenectomy is weakly recommended for advanced RGC involving the greater curvature³⁰. Conversely, not performing splenic hilar dissection with splenectomy is also weakly recommended when the tumor does not invade the greater curvature. In practice, commonly involved nodal stations in RGC include No. 19, 11p, 3, 4sb, and 7. In patients with prior Billroth-II reconstruction, station No. 13 and 14v should also be considered due to potential jejunal mesenteric drainage^31,32. Therefore, a modified D2 or selective lymphadenectomy strategy is generally preferred, based on tumor location, route of previous reconstruction, and feasibility of dissection in fibrotic or adhesive fields. The goal is to ensure oncologic radicality while minimizing unnecessary surgical risks³³. In cases where the tumor invades adjacent organs, laparoscopic surgery should continue to follow standard oncologic principles. En bloc resection of involved structures, such as the spleen or the pancreatic tail, should be performed when necessary to achieve R0 resection and ensure complete tumor clearance. If necessary, perform a conversion to open surgery.

Digestive tract reconstruction is also one of the difficulties of LRG. It is typically accomplished using a Roux-en-Y esophagojejunostomy combined with jejunojejunostomy, which helps prevent bile reflux and restore gastrointestinal continuity. Key technical considerations include ensuring that the anastomosis is tension-free and well-perfused, which can be achieved by mobilizing 6-8 cm of the distal esophagus and appropriately lengthening the Roux limb with mesenteric release. Placement of protective drains around the anastomosis is recommended to facilitate postoperative monitoring and reduce the risk of complications.

Although the mean postoperative hospital stay was 12.20 ± 5.63 days, it is noteworthy that the prolonged length of stay was primarily attributed to a single patient who developed a postoperative pulmonary infection. Most patients were discharged within approximately 7-9 days following surgery. Therefore, the average value may not accurately reflect the typical recovery course. Similarly, the observed postoperative complication rate of 20.0% was skewed by this single event. Given the limited sample size, this rate lacks statistical significance and should be interpreted with caution. The actual complication incidence in a larger cohort is likely to be lower. Therefore, due to the small sample size, this study serves primarily as a technical demonstration rather than an outcome study. More clinical researches are needed to confirm these outcomes.

In conclusion, this study systematically details the techniques of LRG for RGC and provides supplementary insights into the existing research data on these techniques. Accumulating evidence confirms its safety and oncological adequacy comparable to open surgery, with added benefits of reduced perioperative bleeding, stress response, and accelerated recovery. Ongoing surgeon training, technical refinement, and multicenter randomized controlled trials are crucial for validating long-term outcomes and promoting wider application. Looking ahead, more patients with RGC are expected to undergo LRG. Surgeon expertise and intraoperative judgment remain pivotal for the successful implementation of these procedures, and they should be performed at high-volume centers by experienced teams.