Abstract
Background/Aim: We evaluated the clinical impact of textbook outcome (TO) in patients with stage I gastric cancer (GC) who underwent minimally invasive surgery (MIS). Moreover, we identified the risk factors associated with achieving TO in these patients.
Patients and Methods: Patients were selected from the database of the Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital between 2005 and 2025. Our definition of TO comprised 10 items: complete (potentially curative) resection, R0 resection, retrieval of more than 16 lymph nodes, no intraoperative complications, no severe postoperative complications (Clavien-Dindo grade III or higher), no reintervention after surgery, no unplanned ICU/HCU admission, no readmission within 30 days after discharge, no prolonged hospital stay (defined as more than 21 days after surgery), and no mortality within 30 days after surgery.
Results: We analyzed 889 patients who underwent MIS and were pathologically diagnosed with stage I GC. Among them, 621 patients (69.8%) achieved TO, whereas 268 patients (30.2%) did not. The most frequent reason for failure to achieve TO was prolonged hospital stay (>21 days after surgery) (17.5%), followed by postoperative surgical complications (15.4%). In the multivariate analysis, age [odds ratio (OR)=1.619), BMI (OR=1.849), and type of gastrectomy (OR=1.674) were identified as independent risk factors for failure to achieve TO. The 5-year overall survival (OS) rate was 97.5% in patients who achieved TO and 94.7% in those who did not, showing a significant difference between the two groups (p=0.041).
Conclusion: The TO achievement rate was approximately 70%, and failure to achieve TO was associated with age, preoperative BMI, and type of gastrectomy. Achievement of TO was associated not only with favorable short-term outcomes but also with improved long-term oncological outcomes.
Introduction
Gastric cancer (GC) is the fifth most common cancer and the fourth leading cause of cancer-related death worldwide (1, 2). Gastrectomy with lymphadenectomy is the standard treatment for resectable GC (3, 4). The prognosis of resectable GC has gradually improved with the introduction of minimally invasive surgery (MIS) and advances in perioperative care (5, 6). The 5-year survival rate for stage I GC has been reported to range from 90% to 95%. Although the prognosis of stage I GC is generally excellent, some patients experience recurrence even after curative gastrectomy. Once recurrence occurs, the prognosis is poor, with a median survival of approximately 10-14 months (7, 8). To further improve survival outcomes in stage I GC, it is important to identify factors that affect prognosis in these patients.
Recently, the quality of the perioperative clinical course has been shown to influence not only short-term oncological outcomes but also long-term survival in various malignancies (9, 10). Textbook outcome (TO) was developed as a composite measure to evaluate the quality of perioperative surgical care (11, 12). TO includes multiple perioperative parameters and has been applied to various malignancies. In 2017, the Dutch Upper Gastrointestinal Cancer Audit (DUCA) defined TO for GC, incorporating 10 short-term surgical outcomes: curative resection, absence of intraoperative complications, R0 resection, adequate lymph node retrieval, absence of severe postoperative complications, no reintervention after surgery, no unplanned intensive care unit admission, no readmission, no prolonged hospital stay, and no mortality (13). Previous studies have demonstrated that achievement of TO is associated with improved postoperative survival (14-16).
In this study, we evaluated the clinical impact of TO in patients with stage I GC who underwent MIS. Furthermore, we investigated the risk factors associated with achieving TO in these patients and examined whether achievement of TO influences survival in stage I GC.
Patients and Methods
Patients. Patients were selected from a prospectively maintained database at the Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan. All patients were consecutively registered in the database. Eligibility criteria were as follows: (i) histologically confirmed gastric adenocarcinoma; (ii) curative laparoscopy-assisted gastrectomy (LAG) or robotic-assisted gastrectomy (RAG) as the primary treatment between 2005 and 2025; and (iii) pathologically diagnosed stage I disease according to the third English edition of the Japanese Classification of Gastric Carcinoma (17).
Surgical procedures. In principle, all patients underwent distal, proximal, or total gastrectomy with lymph node dissection. D1 or D1+ lymphadenectomy was indicated for cT1N0 tumors, whereas D2 lymphadenectomy was indicated for cN+ or cT2-T4 tumors, regardless of the surgical approach.
Perioperative care. All patients received standardized perioperative management. Cefazolin (1 g) was administered 30 min before skin incision, repeated every three hours during surgery, and administered at a dose of 2 g on postoperative day (POD) 1. Patients were allowed a normal diet until midnight on the day before surgery. Oral water intake was initiated on POD 1. Solid food intake began on POD 3, starting with rice gruel and soft foods and progressing in three steps to a regular diet (18).
Textbook outcome. TO was defined based on the following 10 criteria: complete (potentially curative) resection, R0 resection, retrieval of more than 16 lymph nodes, absence of intraoperative complications, absence of severe postoperative complications (Clavien-Dindo grade III or higher), no reintervention after surgery, no unplanned intensive care unit (ICU)/high care unit (HCU) admission, no readmission within 30 days after discharge, no prolonged hospital stay (>21 days after surgery), and no mortality within 30 days after surgery.
Statistical analysis. Tumor staging was assessed according to the 15th edition of the Japanese Classification of Gastric Carcinoma. Overall survival (OS) was estimated using the Kaplan-Meier method and compared using the log-rank test. Univariate and multivariate logistic regression analyses were performed to identify risk factors associated with failure to achieve TO. Comparisons between groups were conducted using the chi-square test. Variables with significance in univariate analysis were entered into the multivariate model using backward elimination. All statistical tests were two-tailed, and p values <0.05 were considered statistically significant. Statistical analyses were performed using SPSS software (version 29.0 J Win; SPSS, Chicago, IL, USA). This study was approved by the Institutional Review Board of the Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital.
Results
Patient characteristics and achievement of textbook outcome. A total of 889 patients who underwent minimally invasive gastrectomy and were pathologically diagnosed with stage I GC were analyzed. The median age was 69 years (range=27-91 years). There were 610 male and 279 female patients. The median body mass index (BMI) was 23.0 kg/m2 (range=14.4-34.9 kg/m2). LAG was performed in 798 patients, and RAG in 91 patients. Among the 889 patients, 621 (69.8%) achieved TO, whereas 268 (30.2%) failed to achieve TO. The most frequent reason for failure to achieve TO was prolonged hospital stay (>21 days after surgery) (156/889, 17.5%), followed by postoperative surgical complications (137/889, 15.4%) (Figure 1). Comparison of patient backgrounds between the TO achievement group and the TO failure group revealed significant differences in age, BMI, and the incidence of vascular disease and diabetes mellitus. Patients who failed to achieve TO were older (71 vs. 68 years, p<0.001) and had a higher BMI (23.5 vs. 22.5 kg/m2, p<0.001) than those who achieved TO (Table I). Regarding surgical and pathological findings, significant differences were observed in the type of gastrectomy, operation time, blood loss, and number of harvested lymph nodes. Patients who failed to achieve TO had a higher incidence of total gastrectomy (8.5% vs. 6.7%, p<0.001), longer operation time (263 vs. 251 min, p=0.020), greater blood loss (25 vs. 20 ml, p=0.018), and fewer harvested lymph nodes (31 vs. 37, p<0.001) compared with those who achieved TO (Table II). Although 30-day mortality was similar between the two groups, surgical complications, reoperation rates, and postoperative hospital stay were significantly higher or longer in the TO failure group (Table III).
Textbook outcome results.
Baseline characteristics of the study patients.
Surgical and pathological findings.
Postoperative clinical outcomes.
Risk factor analysis for achievement of TO. Table IV presents the risk factor analysis for failure to achieve TO. Univariate analysis identified age, BMI, type of gastrectomy, and vascular disease as significant factors. Multivariate analysis demonstrated that age [OR=1.619; 95% confidence interval (CI)=1.172-2.236; p<0.001], BMI (OR=1.849; 95% CI=1.364-2.508; p<0.001), and type of gastrectomy (OR=1.674; 95% CI=1.385-2.024; p<0.001) were independent risk factors for failure to achieve TO.
Risk factors analysis for achievement of textbook outcome.
Comparison of survival between TO achievement and TO failure groups. Figure 2 shows the OS curves for patients who achieved TO and those who failed to achieve TO. The 1-, 3-, and 5-year OS rates were 99.8%, 98.3%, and 97.5%, respectively, in the TO achievement group, compared with 97.7%, 96.8%, and 94.7%, respectively, in the TO failure group. A significant difference in OS was observed between the two groups (p=0.041).
Comparison overall survival between the patients with textbook outcome achievement and those without textbook outcome achievement.
Discussion
The aim of the present study was to evaluate the clinical impact of TO in patients who underwent MIS for GC. The major findings were that the TO achievement rate was approximately 70% among patients with stage I GC who underwent MIS, and that age, BMI, and type of gastrectomy were independent risk factors for failure to achieve TO. Furthermore, achievement of TO was significantly associated with improved OS. These findings suggest that achieving TO may contribute to improved survival in patients with GC. Therefore, careful perioperative management is particularly important in patients with risk factors for failure to achieve TO, in order to improve both TO achievement and survival outcomes.
In the present study, the TO achievement rate was 69.8% among patients with GC who underwent MIS. A previous review of 40 studies evaluating TO in GC surgery reported a median TO achievement rate of 56.5% (range=38.5%-73.7%). Our results are comparable to those reported in recent studies (19). Ramos et al. evaluated the clinical impact of TO in 681 patients with GC who underwent gastrectomy between 2009 and 2022 in Brazil (20). They reported a TO achievement rate of 65.2%. The most common reasons for failure to achieve TO were major surgical complications (47.3%), followed by prolonged hospital stay (>21 days) (37.6%). Similarly, Sędłak et al. analyzed 1,700 GC patients who underwent gastrectomy between 2017 and 2022 in Europe and reported a TO achievement rate of 68.5% (21). In their study, postoperative complications (12.4%) and prolonged hospital stay (11.8%) were the most frequent factors contributing to failure to achieve TO.
Although the overall TO achievement rates were similar between our study and previous reports, there were discrepancies in the factors contributing most to failure. In our study, prolonged hospital stay was the most common reason for failure, followed by severe postoperative complications, whereas other studies reported severe postoperative complications as the predominant factor. Several explanations may account for this difference. First, surgeons may be cautious about early discharge after gastrectomy because major complications can occur in a delayed fashion. A recent study of patients undergoing colonic surgery showed that only half of the patients were discharged when discharge criteria were met, and 43% remained hospitalized based on the surgeon’s judgment (22). Second, differences in post-discharge healthcare systems may contribute to this discrepancy. In our study, almost all patients were discharged home, whereas in other countries, discharge to home with healthcare support or to a nursing facility may be more common.
In the present study, age, BMI, and type of gastrectomy were identified as independent risk factors for failure to achieve TO, with odds ratios of 1.619, 1.849, and 1.674, respectively. Four previous studies have investigated risk factors for TO achievement. Bobrzynski et al. analyzed 1,743 patients with GC (TO rate: 29%) and reported that age, ASA score, tumor size and location, pathological T status, lymph node metastasis, type of gastrectomy, extent of lymphadenectomy, and combined organ resection were associated with TO (23). Hirata et al. demonstrated that age was a risk factor in a cohort of 161 patients with GC (24). Ramos et al. identified ASA status, Charlson Comorbidity Index (CCI), type of lymphadenectomy, and elective ICU admission as risk factors in 681 patients with GC (TO rate: 65.2%) (20). Sędłak et al. reported that age, ASA score, T status, neoadjuvant chemotherapy, type of gastrectomy, and extent of lymphadenectomy were significant risk factors in 1,700 patients with GC (TO rate: 68.5%) (21). Among these five studies, including ours, four identified age as a common risk factor for failure to achieve TO after gastrectomy. These findings suggest that particular attention should be paid to elderly patients to improve TO achievement.
We also demonstrated a significant difference in survival between patients who achieved TO and those who did not. Similar findings have been reported previously. Levy et al. analyzed 1,836 patients with GC who underwent gastrectomy between 2004 and 2015 and reported a TO achievement rate of 22% (25). The 3-year OS rate was 74.6% in the TO achievement group compared with 55.0% in the non-achievement group (p<0.001). Cero et al. evaluated 1,293 patients with GC treated between 2014 and 2017 (TO rate: 41.1%) and found that the 3-year OS rate was 72.8% in the TO achievement group versus 55.0% in the non-achievement group; median OS was 36.6 months and 28.1 months, respectively (both p<0.001) (26). Although we were unable to demonstrate that TO was an independent prognostic factor for OS due to the low number of events in stage I GC, previous studies have shown that TO is an independent prognostic factor in patients undergoing curative gastrectomy. Roh et al. evaluated 395 patients with GC (pathological stage I-III) who underwent robotic or laparoscopic total gastrectomy and reported that TO was an independent prognostic factor for both OS [hazard ratio (HR)=2.46; 95% CI=1.28-4.73; p=0.007] and relapse-free survival (HR=2.33; 95% CI=1.31-4.15; p=0.004) (27). Other studies have reported similar findings. Therefore, achievement of TO may serve as a promising prognostic indicator in GC.
Limitations. First, this was a retrospective single-institution study conducted at a specialized cancer center, which may introduce selection bias. Second, there may be a time-related bias, as patients were included over a long study period (2005-2025). During this time, perioperative management evolved considerably, including the introduction of enhanced recovery after surgery (ERAS) protocols. These changes may have influenced outcomes such as length of hospital stay and, consequently, TO achievement. Despite these limitations, few studies have specifically evaluated TO in patients with GC undergoing MIS. Therefore, our findings provide clinically meaningful insights into the relationship between TO and outcomes in GC treatment.
In conclusion, the TO achievement rate was approximately 70%, and failure to achieve TO was associated with age, preoperative BMI, and type of gastrectomy. Achievement of TO was associated with improved short-term and long-term oncological outcomes in patients with stage I GC undergoing MIS.
Acknowledgements
The Authors express their sincere gratitude to Ms. Emiko Saito for her excellent data management.
Footnotes
Authors’ Contributions
TA and HC made substantial contributions to conception and design. TA, HC, KH, and HS made substantial contributions to the acquisition, analysis, and interpretation of data. TA and HC were involved in drafting the manuscript and revising it critically for important intellectual content. All Authors provided final approval for the version to be published. Each author participated sufficiently in the work to take public responsibility for appropriate portions of the content and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All Authors have read and approved the final manuscript.
Conflicts of Interest
The Authors declare no conflicts of interest in association with the present study.
Artificial Intelligence (AI) Disclosure
During the preparation of this manuscript, a large language model (ChatGPT, OpenAI) was used solely for language editing. No sections involving the generation, analysis, or interpretation of research data were produced by generative AI. All scientific content was created and verified by the authors. Furthermore, no figures or visual data were generated or modified using generative AI or machine learning-based image enhancement tools.
- Received February 12, 2026.
- Revision received March 10, 2026.
- Accepted March 17, 2026.
- Copyright © 2026 The Author(s). Published by the International Institute of Anticancer Research.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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