Wang SD, Chang YZ, Ding SK, Bian ZM, Xie YB. Prognosis of signet-ring cell carcinoma after proximal gastrectomy was comparable to total gastrectomy but with better nutrition status. World J Gastrointest Oncol 2026; 18(5): 117410 [DOI: 10.4251/wjgo.v18.i5.117410]
Corresponding Author of This Article
Yi-Bin Xie, Postdoc, Professor, Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, No. 18 Panjiayuan Nanli, Chaoyang District, Beijing 100021, China. yibinxie@cicams.ac.cn
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Oncology
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Retrospective Cohort Study
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May 15, 2026 (publication date) through May 14, 2026
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World Journal of Gastrointestinal Oncology
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1948-5204
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Wang SD, Chang YZ, Ding SK, Bian ZM, Xie YB. Prognosis of signet-ring cell carcinoma after proximal gastrectomy was comparable to total gastrectomy but with better nutrition status. World J Gastrointest Oncol 2026; 18(5): 117410 [DOI: 10.4251/wjgo.v18.i5.117410]
Shun-Da Wang, Ya-Zhou Chang, Yi-Bin Xie, Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
Shi-Kang Ding, Department of General Surgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences/Peking Union Medical College, Beijing 100021, China
Zhi-Min Bian, Department of Comprehensive Unit, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
Co-corresponding authors: Zhi-Min Bian and Yi-Bin Xie.
Author contributions: Wang SD contributed to study conception and manuscript writing and data analysis; Chang YZ and Ding SK contributed to data collection; Bian ZM and Xie YB contributed to clinical treatment and diagnosis. All authors contributed to the article and approved the submitted version. Wang SD and Chang YZ contributed equally to this work as co-first authors. This manuscript involves multidisciplinary collaboration between surgical and medical oncology. Xie YB and Bian ZM contributed equally to study conception, data interpretation, and manuscript revision. This co-corresponding authorship reflects their complementary expertise and shared responsibility, ensuring the paper’s clinical relevance and scientific rigor. This arrangement is common in complex clinical oncology research.
Supported by Hubei Chen Xiaoping Science and Technology Development Foundation, No. CXPJJH123010-6; and Wu Jieping Medical Foundation, No. 320.6750.14137.
Institutional review board statement: The Ethics Committee of the National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, No. 25/191-5137.
Informed consent statement: This retrospective study was approved by the Ethics Committee of National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences, and the need for informed consent was waived.
Conflict-of-interest statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
STROBE statement: The authors have read the STROBE Statement-checklist of items, and the manuscript was prepared and revised according to the STROBE Statement-checklist of items.
Data sharing statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Corresponding author: Yi-Bin Xie, Postdoc, Professor, Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, No. 18 Panjiayuan Nanli, Chaoyang District, Beijing 100021, China. yibinxie@cicams.ac.cn
Received: December 8, 2025 Revised: February 8, 2026 Accepted: March 12, 2026 Published online: May 15, 2026 Processing time: 158 Days and 15.8 Hours
Abstract
BACKGROUND
Currently, there is no consensus on whether proximal gastrectomy (PG) or total gastrectomy (TG) should be used for upper gastric signet-ring cell carcinoma (SRCC), and the long-term oncological outcome and postoperative nutritional status is still debatable.
AIM
To provide evidence for better clinical decisions, oncological safety and nutritional status of SRCC patients post-PG or -TG were compared.
METHODS
Patients who underwent PG or TG at a single institution between June 2014 and June 2018 were included. Inclusion and exclusion criteria were defined, and the endpoint was long-term surgical outcomes, including overall survival (OS), postoperative nutritional status, and complications. Prognostic factors were evaluated using univariate and multivariate Cox proportional-hazards regression models.
RESULTS
Those undergoing TG presented with a larger tumor size and later pathological stage compared with the PG group (P < 0.001). Propensity score matching eliminated differences in clinicopathological factors. Finally, 94 PG and 130 TG group members were analyzed. Our findings revealed that there was no significant difference in OS (47.7% vs 53.1%, P = 0.059), complications, and recurrence/relapse incidence between the PG and TG groups. Further, there were no notable differences in nutritional parameters between the TG and PG groups during a 5-year follow-up. However, postoperative malnutrition and anemia were significantly elevated in the TG group compared with the PG group (P = 0.014, P = 0.005, respectively).
CONCLUSION
For SRCC, PG was more aggressively recommended because it manifested similar prognosis and better nutritional status compared with that for TG.
Core Tip: The optimal surgical approach for upper gastric signet-ring cell carcinoma (SRCC)-proximal gastrectomy (PG) or total gastrectomy (TG)-remains controversial. This study specifically addressed this gap by comparing the outcomes of PG and TG for SRCC located in the upper stomach. Our results demonstrated that PG offered a prognosis comparable to that of TG while providing superior postoperative nutritional status. Therefore, for patients with upper SRCC, PG represents a viable and favorable surgical option.
Citation: Wang SD, Chang YZ, Ding SK, Bian ZM, Xie YB. Prognosis of signet-ring cell carcinoma after proximal gastrectomy was comparable to total gastrectomy but with better nutrition status. World J Gastrointest Oncol 2026; 18(5): 117410
Gastric cancer (GC) is the fifth most common malignant tumor and fourth leading cause of cancer-related death[1]. Although the overall prevalence of GC is decreasing, the incidence of signet-ring cell carcinoma (SRCC) subgroups is rising[2,3]. SRCC is a type of adenocarcinoma where > 50% of the tumor consists of extracellular mucinous pools[4]. SRCC and non-SRCC are considered to be distinct biological entities originating from different processes of carcinogenesis[5]. SRCC is increasingly diagnosed and often located in the proximal stomach[3]. Previous studies have indicated that SRCC or diffuse-type GC has a worse prognosis compared with other GCs because of its poorly cohesive nature and tendency to invade via submucosal and subserosa pathways[6-8].
The surgical treatment of upper GC, especially SRCC, is complex. Total gastrectomy (TG) with lymphadenectomy has long been the gold standard for upper gastric tumors, ensuring adequate resection margins and lymph node dissection[9]. However, TG inevitably leads to significant postoperative sequelae, including weight loss, malnutrition, anemia, dumping syndrome, and alterations in bone metabolism, profoundly impacting the quality of life of the patient[10]. Proximal gastrectomy (PG), which preserves the distal stomach, has emerged as a function-preserving alternative for carefully selected tumors in the upper stomach. The theoretical advantages of PG include better maintenance of reservoir capacity, improved nutrient absorption, and potentially enhanced quality of life[11-13].
Despite these functional benefits, the oncological safety of PG compared with TG for SRCC has been debated for the following reasons: The adequacy of lymph node dissection along the distal stomach, the risk of local recurrence, and the long-term survival equivalence[14]. Although several studies and meta-analyses have suggested a comparable duration of overall survival (OS) between PG and TG cases, many of these reports encompass heterogeneous histological types of GC[15]. Studies specifically focusing on SRCC of the upper stomach have been less conclusive. However, there is currently no specific and well-defined standard of treatment for SRCC, and it remains unclear which surgical procedure is more beneficial for long-term survival and postoperative nutrition in patients with SRCC. This study specifically assesses the comparative outcomes of PG vs TG for patients with SRCC located in the upper stomach. We hypothesize that PG provides equivalent long-term oncological outcome compared with TG while offering superior preservation of postoperative nutritional status for appropriately selected SRCC cases in the proximal stomach. We conducted a large-scale retrospective study at a single center in China, analyzing survival outcomes, nutritional parameters, and postoperative complications to determine the most beneficial surgical procedure for treating SRCC.
MATERIALS AND METHODS
Study participants
In total, 715 patients with SRCC who received partial or TG at our center, from January 2014 to June 2018, were included in this study. The inclusion criteria for this study were as follows: Total or PG with D2 dissection performed by senior surgeons in accordance with the Japanese GC treatment guidelines, histological confirmation of primary SRCC, confirmation of the pathological results by two pathologists, no history of other malignant tumors, at least two follow-up examinations conducted, and an interval exceeding 3 months between the first follow-up examination and surgery. Patients who were not successfully followed up were eliminated from our study. This work has been reported in line with the Strengthening the Reporting of Observational Studies in Epidemiology guidelines[16].
Surgical method
The multidisciplinary treatment group including medical oncologists, surgeons, radiologists and pathologists collaboratively formulated treatment plans for patients, according to the preoperative assessment of contrast-enhanced chest-abdomen-pelvis computed tomography (CT), upper gastrointestinal endoscopy and other examinations. The selection of a particular surgical approach was informed by the “Japanese gastric cancer treatment guidelines (ver.5)” and the clinical experience of the surgeon. TG was typically indicated for patients with tumors larger than 4 cm in diameter, deeper invasion, or more advanced stages. Conversely, PG may be considered for patients with small, well-localized tumors where a negative distal resection margin could be assured. Esophagogastrostomy and esophagojejunostomy were performed by the overlap method. For curable cT2-T4 tumors as well as cT1N+ tumors, it was recommended to perform TG or PG with D2 lymph node dissection. Additionally, all patients with tumor node metastasis stage II-III were advised to receive postoperative adjuvant chemotherapy while others with advanced stage cancer underwent a surgical procedure following neoadjuvant chemotherapy.
Study endpoint
The endpoint was long-term overcomes including complications, postoperative nutritional status and OS where OS was defined as the period from the date of surgery to that of death. The assessment of long-term nutritional status involved measuring body weight, body mass index (BMI), and laboratory blood indicators, including total protein, pre-albumin, hemoglobin levels and the red blood cell (RBC) count.
Data collection and follow-up
Data were retrospectively collected from hospital electronic medical records. All patients underwent regular postoperative re-examinations at the hospital every three months for the first 2 years after surgery, every 6 months for 3-5 years post-surgery, and annually after 5 years. All postoperative follow-up examinations comprised a physical exam, peripheral blood laboratory tests, chest CT, abdominal CT, pelvic CT or magnetic resonance imaging, and positron emission tomography if required. Additionally, the researchers conducted telephone interviews to assess the general situation of each patient. The Clavien-Dindo classification was used to assess the severity of postoperative complications[17].
Statistical analysis
Clinical data are presented as the mean ± SD. We compared categorical and continuous variables using the χ2 test and student’s t test, respectively. The Kaplan-Meier method was utilized to compare survival. The Log-rank test was also employed. The Cox proportional hazard model was used to verify independent prognostic factors. A P value < 0.05 was considered significant. Statistical analyses were conducted by employing SPSS software version 20.0 (SPSS Inc., Chicago, IL, United States), R software version 4.0.2 (R Foundation for Statistical Computing, Vienna, Austria) and GraphPad Prism 7 software (GraphPad Software, San Diego, CA, United States).
RESULTS
Clinicopathological features
This study initially consisted of 715 patients with SRCC admitted to our hospital between January 2014 and June 2018 who underwent gastrectomy and included 399 TG and 316 PG cases. As shown in Table 1, we conducted an analysis of demographic and clinicopathological characteristics regarding patients with upper gastric SRCC, and found that the surgical procedure, Lauren type, Bormann type, tumor size, neoadjuvant therapy and pathological stage between these two groups (PG vs TG) were significantly different (P < 0.005). We observed that patients with SRCC who underwent TG presented with a larger tumor size and later pathological stage compared with those undergoing PG (P < 0.001) (Table 1). A logistic regression model was used to conduct propensity score matching (PSM) analysis and covariates that were closely matched were identified. Finally, there were 94 PG and 130 TG cases included in our study. The clinicopathological characteristics of patients after PSM analysis are presented in Table 2.
Table 1 Demographic and clinicopathological characteristics of patients with upper gastric signet-ring cell carcinoma who underwent total gastrectomy or proximal gastrectomy, n (%).
Table 2 Demographics and clinicopathological characteristics of patients with upper gastric signet-ring cell carcinoma who underwent total gastrectomy or proximal gastrectomy after propensity score matching, n (%).
The incidence of postoperative complications is shown in Table 3. There were no significant differences in the incidence of overall short-complications between the two groups of patients with SRCC (P = 0.954). However, the PG group experienced a significantly higher overall incidence of anastomotic stenosis in comparison with the TG group (P = 0.036). Besides, the incidence levels of anastomotic leakage, duodenal stump leakage, abdominal infection, and hemorrhage were similar between the two groups. Regarding long-term complications, our results revealed that the PG group had a significantly higher incidence of reflux esophagitis compared with the TG group (P < 0.001). Further, compared with the PG group, the TG group had a significantly higher prevalence of malnutrition and anemia (P = 0.014, P = 0.005, respectively).
Table 3 Postoperative complications of patients with upper gastric signet-ring cell carcinoma who underwent total gastrectomy or proximal gastrectomy, n (%).
The changes observed in the postoperative nutritional status of patients are shown in Figure 1. There were no notable differences in changes in per cent BMI and per cent body weight values at each follow-up time point between the two groups. The changes in per cent BMI and per cent body weight values of the two groups decreased rapidly within the first 3 months and tended to be stable after 1 year, and then increased slightly after 2-3 years (Figure 1A and B). There were no notable differences in protein and pre-albumin level changes between the two groups (P > 0.05) (Figure 1C and D). The hemoglobin levels in the PG group were slightly higher than those in the TG group at each follow-up time point during the 5 years after surgery, with statistical significance observed at 6 months post-surgery (P < 0.05). Regarding the RBC count, it was higher in the PG compared with the TG group at each follow-up time point in 5 years post-surgery but did not achieve statistical significance (Figure 1E and F). Overall, nutritional indicators in PG cases were somewhat better than those in TG cases after 5-year follow-ups, especially for hemoglobin levels and RBC counts: This was consistent with the higher incidence of anemia in the TG compared with the PG group, as mentioned in the complications section above.
Figure 1 Changes in the nutritional status trend within 5 years post-surgery among patients in the total gastrectomy and proximal gastrectomy groups.
A: Body mass index; B: Weight; C: Total protein; D: Prealbumin; E: Hemoglobin; F: Red blood cells. BMI: Body mass index; TP: Total protein; PALB: Prealbumin; HB: Hemoglobin; RBC: Red blood cells; TG: Total gastrectomy; PG: Partial gastrectomy; NS: Not significant. aP ≤ 0.05.
Survival outcome
After follow-up screening, a PSM analysis was conducted that resulted in a total of 224 patients with SRCC being included in the survival analysis. There were no statistically significant differences in OS between the TG and PG groups in patients with SRCC (P = 0.059; Figure 2). However, Kaplan-Meier analysis revealed that lymphatic invasion, perineuronal invasion, T stage, N stage, adjuvant therapy, and relapse were prognostic indicators in the univariate analysis (P < 0.05; Table 4). Further, multivariate Cox regression analysis revealed that T stage and relapse were risk factors for OS among patients with SRCC [hazard ratio (HR) = 3.598, 95% confidence interval (CI): 2.582-6.411, P < 0.001; HR = 2.37, 95%CI: 1.523-3.688, P < 0.001] (Table 4).
As for postoperative recurrence, 34 of 224 (15.2%) patients relapsed after surgery, 16 belonged to the PG and 18 to the TG group; the differences were not significant (P = 0.71) (Table 5). In situ relapse, regional lymph node, hematogenous, and dissemination recurrences developed in five (2.2%), 11 (4.9%), 10 (4.5%), and eight (3.6%) patients, respectively. Taken together, our results revealed that the choice of surgical approach (either PG or TG) was not associated with survival. This finding implies that the organ-preserving PG approach was equivalent to TG for treating SRCC in terms of oncological safety.
Table 5 A comparison of cancer recurrence between the total gastrectomy and proximal gastrectomy groups, n (%).
The incidence of upper gastric SRCC is increasing, and the long-term prognosis of various surgical procedures employed for treating SRCC remains unclear in the literature[18,19]. Therefore, we conducted this study to investigate the long-term impact of different surgical procedures used to treat upper gastric SRCC, including survival, complications, and postoperative nutritional status. Our findings revealed that there was no statistically significant difference in OS values between the TG and PG groups. We also verified by Cox regression analysis that the type of surgical approach employed was not an important factor for determining prognosis for patients with upper gastric SRCC. Additionally, the postoperative nutritional status in the PG group was slightly better than that in the TG group, exhibiting reduced malnutrition and anemia.
The survival outcome of GC in the upper third of the stomach when treated via various surgical approaches (PG or TG) has not reached an agreement in the field of gastrointestinal tumors. Traditionally, TG typically implies a more thorough lymph node dissection and a lower risk of recurrence and metastasis. However, numerous studies have reported that PG was not less effective than TG with regard to prognosis. Conversely, a retrospective study has shown that the 5-year OS of patients with SRCC who underwent PG was primarily consistent with those of the TG group[18]. Another study conducted in the United States reported that patients with SRCC were more likely to undergo TG treatment (25.5% vs 20.9%; P < 0.0001), while patients with SRCC who underwent PG exhibited better OS compared with those who underwent TG (P < 0.0001)[19]. A previous study by our center found that among patients with esophagogastric junction GC at a similar stage, the overall 5-year survival was similar between the PG and TG groups, with no statistically significant differences[20]. Following neoadjuvant chemotherapy for GC in the upper third of the stomach, the PG approach with tubular stomach reconstruction is comparable to TG in terms of surgical safety and long-term oncological outcomes[21]. In this study, we utilized PSM analysis based on pathological characteristics to compare the survival outcomes of PG and TG groups, revealing no significant differences in OS. Although the follow-up time reported in the current study is insufficient, we plan to publish updated results with longer-term survival data in the future.
The results of our study also compared the postoperative complications of PG and TG for SRCC; however, our analysis showed that there was no statistically significant difference in the overall complication rate, similar to previous reports. The significantly increased occurrence of reflux esophagitis and anastomotic stricture after PG has been well-documented as a challenge linked to this organ-preserving method. Resection of the gastroesophageal junction disrupted the natural barrier of anti-reflux, while the reduced gastric capacity increased the propensity for bile and acid reflux into the remnant esophagus. Further, the typical esophagogastrostomy reconstruction created an anastomosis under higher tension and subject to corrosive refluxate, contributing to the development of fibrotic strictures. These conclusions are consistent with a number of comparative studies as well as meta-analyses[22,23]. Additionally, our study found a slightly higher incidence of malnutrition and anemia in the TG compared with the PG group. TG eliminated intrinsic factor production and the primary site for acid-mediated iron solubilization, directly impairing the absorption of vitamin B12 and non-heme iron, contributing significantly to weight loss and malabsorption of micronutrients. Research by Park et al[24] has demonstrated significantly lower serum albumin, hemoglobin, iron, and vitamin B12 levels, alongside higher rates of nutritional intervention, in TG compared with PG.
For patients who received gastrectomy, postoperative nutrition was an important indicator and a problem of significant concern. Previous studies commonly assessed postoperative BMI and weight changes as nutritional indicators. Two retrospective studies conducted in Korea showed that patients with GC in the middle-to-upper third of the stomach who underwent either PG or TG experienced a reduction in BMI and body weight during the initial 3 to 6 months post-operative period, followed by a gradual stabilization, with similar changes observed in BMI and body weight between the two patient groups defined in the current study[25,26]. In this study, we observed a similar trend in BMI% and body weight% changes within 5 years postoperatively. Next, we compared postoperative nutritional status using hematological examinations as evaluation indicators for TG and PG procedures. The hemoglobin levels and RBC counts in the TG group were lower than those in the PG group postoperatively at each follow-up time point within 5 years. This finding was similar to that mentioned in the “short and long term complications” sub-section of the Results section of the current report in that the TG group showed more malnutrition and anemia than the PG group. Kosuga et al[27] also showed significantly lower levels of postoperative hemoglobin and total lymphocyte count in the TG group compared with the PG group at 2 years post-surgery, but Ahn et al[11] found no significant differences in the changes of total protein, hemoglobin and albumin between the two groups. These results are not entirely consistent, and the nutritional status changes after different gastrectomy procedures need further study to be verified. As for a physiological mechanism, PG maintains gastric reservoir capacity and regulated emptying via the preserved pylorus, reducing occurrence of the dumping syndrome. Further, PG primarily retains the secretion of gastric acid and intrinsic factor, which supports protein digestion and the absorption of iron, calcium, and vitamin B12[24]. Collectively, these preserved functions enhance the absorption of both macronutrients and micronutrients, leading to a better long-term nutritional status.
This study has several limitations that are worth discussing. First, the relatively small sample size may restrict the statistical power and generalizability of our results to a certain extent. Our analysis, based on retrospective data collected at a single institution, was not representative. Second, the short duration of the follow-up restricts our ability to assess long-term outcomes. The follow-up was not continuous for all patients, and some follow-up data were not available. Nevertheless, the follow-up rates observed in this study are similar to those found in other long-term studies. The relatively short follow-up period may limit the assessment of long-term survival outcomes, but the current data already provided critical evidence regarding perioperative safety. Third, the presence of partial or missing data in key variables may have introduced a selection bias. There was a partial reduction in the number of patients returning to the hospital for follow-up examinations in the later stages of the study, which led to a relative decrease in statistical power. Therefore, a well-designed future prospective study is required to deal with these shortcomings.
CONCLUSION
In conclusion, this study comprehensively compared the long-term outcomes of gastrectomy via either TG or PG in patients with upper gastric SRCC. PG was comparable to TG in terms of long-term oncological outcome but displayed a better nutritional status compared with patients who underwent TG for upper gastric SRCC.
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