Quality of life and survival of achieving textbook outcome for resectable esophageal squamous cell carcinoma

Introduction

Esophageal squamous cell carcinoma (ESCC) remains one of the most aggressive malignancies worldwide, with a high mortality rate and significant impact on patients’ quality of life (QOL) (1). Despite advances in surgical techniques, chemotherapy, and radiotherapy, the prognosis for patients undergoing esophagectomy remains suboptimal, with a substantial proportion experiencing severe postoperative complications (2). These complications not only affect survival outcomes but also significantly impair patients’ postoperative QOL (3,4). Therefore, there is an urgent need for comprehensive quality control measures to optimize surgical outcome.

In recent years, the concept of “textbook outcome (TO)” has emerged as a multifaceted quality indicator in surgical oncology (5-11). TO represents an ideal surgical result, encompassing a set of critical perioperative and postoperative metrics that, when achieved, signify optimal surgical care. Initially introduced in colorectal surgery, TO has been increasingly applied in esophageal cancer surgery to evaluate the overall quality of surgical interventions (12-14). The TO criteria typically include factors such as complete tumor resection with negative margins, adequate lymph node dissection, absence of severe complications, and timely postoperative recovery. Achieving TO has been associated with improved survival outcomes, but its impact on postoperative QOL remains underexplored.

Postoperative QOL is a critical outcome in cancer surgery, reflecting the physical, emotional, and social well-being of patients following treatment. For esophageal cancer patients, QOL is often significantly affected by complications of surgery, including dysphagia, nutritional deficiencies, and psychological distress. While TO focuses on objective surgical outcomes, its relationship with subjective patient-reported outcomes, such as QOL, is not well understood.

This study aimed to investigate the association between achieving TO and postoperative QOL and survival in patients undergoing esophagectomy for esophageal cancer. By analyzing a cohort of patients who achieved TO versus those who did not, we seek to determine whether TO is a reliable predictor of improved QOL. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1839/rc).

Methods

Patients

This retrospective single-center study utilized prospectively collected patient-reported outcome data from our prospective database REDCap (http://125.71.214.100:888/redcap). The data collection was conducted independently by the researchers, who interpreted the questionnaire items using unified guidelines to identify patients with ESCC who met the inclusion criteria. With the patients’ informed consent, the researchers gathered general data by consulting them and reviewing their medical records during hospitalization. The study population comprised consecutive patients diagnosed with ESCC who underwent minimally invasive McKeown esophagectomy at Sichuan Cancer Hospital between April 2019 and December 2020. Comprehensive baseline demographic and clinical characteristics were systematically collected, including age, gender, body mass index (BMI), comorbidities (specifically diabetes mellitus, hypertension, and coronary artery disease), educational attainment, smoking history, alcohol consumption patterns, tumor localization, clinical staging, Eastern Cooperative Oncology Group performance status (ECOG-PS) scores, American Society of Anesthesiologists (ASA) grade and details of neoadjuvant and adjuvant therapeutic interventions. Pathological staging was determined in accordance with the 8th edition of the American Joint Committee on Cancer (AJCC) Cancer Staging Manual, utilizing diagnostic modalities including endoscopic ultrasonography and computed tomography (CT) imaging (15,16).

To be eligible for inclusion in the study, the patients had to meet the following inclusion criteria: (I) have squamous cell carcinoma; (II) have esophageal cancer located in the thorax; (III) have undergone minimally invasive McKeown esophagectomy; (IV) have a stapled anastomosis; and (V) be aged from 18 to 80 years. For all the included patients, during the minimally invasive McKeown esophagectomy, after the esophagus was disconnected at the neck, the circular stapler anvil was inserted into the proximal esophageal stump, and then the gastric tube was raised to the neck. A small incision was made at the highest point of the gastric tube, and the stapler body was then inserted to complete the end-to-side anastomosis. Patients were excluded from the study if they met any of the following exclusion criteria: (I) had other malignant tumors; (II) had a non-tubular stomach substitute for the esophagus; and/or (III) had a lack of complete clinical data. Neoadjuvant therapy included neoadjuvant chemoradiotherapy, chemotherapy, and radiotherapy received before surgery.

The study was authorized by the Ethics Committee for Medical Research and New Medical Technology of Sichuan Cancer Hospital (No. SCCHEC-02-2023-090) and informed consent was taken from all the patients. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

TO

TO is a composite quality measure that reflects an ideal perioperative and postoperative course. Differing from single-outcome evaluations, the TO requires simultaneous fulfillment of nine perioperative quality targets, reflecting a holistic approach to surgical excellence in esophagectomy. The patients with TO should meet: (I) tumor-negative resection margins; (II) at least 20 lymph nodes retrieved and examined; (III) no intraoperative complication; (IV) no complication of Clavien-Dindo (CD) III or higher grade; (V) no anastomotic leakage (all grades according to Esophagectomy Complications Consensus Group); (VI) no intensive care unit (ICU)/medium care unit (MCU) readmission; (VII) no hospital staying longer than 14 days; (VIII) no in-hospital mortality; (IX) no readmission related to the surgical procedure. The criteria of TO for esophagectomy was according to the international consensus-based update in 2021 (17). The patients were divided into two groups according to whether they achieved TO. Complications of CD III or higher grade refer to those that require invasive procedures such as surgery, endoscopy or interventional radiology to be addressed, or they can pose life-threatening risks, necessitating ICU monitoring or treatment.

Health-related QOL measurements

The European Organization for Research and Treatment of Cancer (EORTC) Quality of Life Questionnaire Core-30 (QLQ-C30) is a validated instrument for evaluating cancer patients’ QOL across multicultural clinical studies (18). Its complementary Chinese adaptation, the EORTC Quality of Life Questionnaire Esophagus-specific Questionnaire (QLQ-OES18), has demonstrated reliability and clinical utility in assessing health-related QOL specifically for ESCC patients in mainland China (19).

The QLQ-C30 contains 30 items organized into 15 domains: five functional scales (physical, role, cognitive, emotional, social), three symptom scales (fatigue, pain, nausea/vomiting), one global health/QOL scale, and six single-item measures. The OES18 supplement comprises 18 items distributed across four multi-item subscales (dysphagia, eating difficulties, reflux, pain) and six individual symptom assessments (saliva swallowing issues, choking, xerostomia, taste alterations, coughing, speech problems).

Following standardized scoring protocols, raw dimension scores were calculated and subsequently standardized through polarization transformation. Trained researchers conducted systematic data collection using uniform interpretation guidelines to identify eligible ESCC cases. With participants’ consent, demographic and clinical data were obtained through structured interviews and medical record review during hospitalization. QOL assessments occurred at five time points: preoperative baseline and postoperative days 7, 30, 90, and 180. Results are presented as mean (standard deviation) for each QOL domain.

Statistical analysis

All the statistical analyses were conducted using statistical package SPSS (25.0 SPSS Inc., Chicago, IL, USA) or R software, version 4.5.0 (R Core Team, Vienna, Austria) and graphs were constructed by GraphPad Prism 9 (GraphPad Software Inc., San Diego, CA, USA). Continuous variables are presented as mean (standard deviation) or median (interquartile range), while categorical variables are presented as numbers (percentages). Group comparisons were made using appropriate tests: Chi-squared or Fisher’s exact test for categorical variables, and Student’s t-test or Mann-Whitney U test for continuous variables. Multivariable logistic regression modeling was used to study the associations between age, sex, BMI, comorbidities, education, smoking history, drinking history, tumor location, pathological stage, ASA grade, ECOG-PS scores, neoadjuvant therapy and adjuvant therapy and TO. A linear mixed-effects model was used to assess the mean score difference (MD) (20,21) in health-related QOL between the two groups before and after surgery, as well as the differences in changes over time between the groups. This model was adjusted based on clinical characteristics, group, time (the survey time points of health-related QOL), and the interaction between the groups and time (all of which were set as fixed effects). Patients and time were set as random effects. The missing data were estimated using the maximum likelihood estimation method. Longitudinal comparisons of each survey time were performed using mixed models. Kaplan-Meier analyses with right censoring using log-rank, Breslow and Landmark tests were performed to determine the effect of TO on overall survival (OS) and disease-free survival (DFS). The analyses were adjusted for the clinical characteristics. To eliminate the impact of the adequacy of lymph node dissection on the QOL, we excluded patients with fewer than 15 lymph nodes dissected and re-performed the mixed model. Only MD ≥10 points was considered clinically relevant (20-22). Otherwise, the difference was considered potentially existing only when P<0.05. For other tests, a two-sided P value <0.05 was considered statistically significant.

Results

Clinical features

Figure 1 provides a flow chart showing the study selection process. The clinical characteristics of all the patients are summarized in Table 1. Figure 2 provided the patients achieving TO and each of the criteria. Serious complications (anastomotic leakage and other complications of CD III +; Table 2) and insufficient lymph node retrieval (<20) were the main barriers to TO. The TO group comprised 123 (of the 385 patients, 31.9%), and the non-TO group comprised 262 patients (68.1%). The achievement of TO was significantly associated with neoadjuvant therapy (P=0.02). There were no significant differences between the two groups in terms of age, sex, BMI, comorbidities, education, smoking history, drinking history, tumor location, clinical stage, ASA grade, ECOG-PS scores, neoadjuvant therapy, and adjuvant therapy.

Figure 1 The flow chart showing the study selection process. TO, textbook outcome.

Figure 2 The bar graphs of the number of patients who achieved and did not achieve TO and the attainment of each criterion. CD, Clavien-Dindo; ECCG, Esophagectomy Complications Consensus Group; ICU, intensive care unit; MCU, medium care unit; TO, textbook outcome.

Factors associated with TO

Multivariable logistic regression analysis was performed to identify patient characteristics predictive of achieving TO, adjusting for all variables presented in the model. As shown in Table 3, most factors examined did not demonstrate a statistically significant association with the likelihood of achieving TO. Two factors were significantly associated with a reduced likelihood of achieving TO: higher ASA grade [III vs. I: odds ratio (OR) 0.17, 95% confidence interval (CI): 0.04–0.76, P=0.02] and receipt of neoadjuvant therapy (yes vs. no: OR 0.54, 95% CI: 0.33–0.90, P=0.02). Specifically, no significant associations were observed for age, sex, BMI, presence of comorbidities, higher education level, smoking history, drinking history, tumor location, pathological stage, ASA grade II, ECOG-PS, or receipt of adjuvant therapy (P>0.05).

Comparison of QOL between TO group and non-TO group

The MD evaluated using the mixed-effects model and the MD evaluated at each time point are presented in the Table 4 and Table S1. Compared with the non-TO group, the TO group had potentially worse social function at 7 days after surgery (unadjusted overall MD =5, 95% CI: 2 to 9, P<0.01; adjusted overall MD =5, 95% CI: 2 to 9, P<0.01; 7-day MD =3, 95% CI: 3.1 to 10, P<0.05; Figure 3A), potentially more financial impact at baseline, 7 days and 90 days after surgery (unadjusted overall MD =−6, 95% CI: −10 to −2, P<0.01; adjusted overall MD =−6, 95% CI: −10 to −2, P<0.01; baseline MD =−3.1, 95% CI: −5.9 to −0.3, P<0.05; 7-day MD =−6.7, 95% CI: −10.0 to −6.7, P<0.05; 90-day MD =−4.6, 95% CI: −8.4 to −0.8, P<0.05; Figure 3B), potentially less trouble with taste from 7 to 90 days after surgery (unadjusted overall MD =5, 95% CI: 1 to 10, P=0.02; adjusted overall MD =5, 95% CI: 1 to 10, P=0.02; 7-day MD =8.5, 95% CI: 3.6 to 13.5, P<0.05; 30-day MD =9.4, 95% CI: 4.6 to 14.2, P<0.05; 90-day MD =4.9, 95% CI: 0.5 to 9.3, P<0.05; Figure 3C).

Figure 3 Comparison of EORTC QLQ-C30 and EORTC QLQ-OES18 between the TO and non-TO groups. Higher scores reflect better function or worse symptoms. Error bars represent 95% CIs. *, the mean score difference between the two groups was significant (P<0.05). CI, confidence interval; EORTC QLQ-C30, European Organization for Research and Treatment of Cancer Quality of Life Questionnaire Core-30; EORTC QLQ-OES18, European Organization for Research and Treatment of Cancer Quality of Life Esophagus-specific Questionnaire; TO, textbook outcome.

Of note, the TO group was observed to have clinically significantly fewer dysphagia 30 days after the surgery (MD =15.1, 95% CI: 8.1 to 22.1, P<0.05), although there was no significant difference in the overall MD (MD =−1, 95% CI: −9 to 7, P=0.79, Figure 3D). In the subsequent survey time points, the dysphagia in the TO group was slightly less than that in the non-TO group (90-day MD =6.2, 95% CI: 1.7 to 10.7, P<0.05; 180-day MD =3.6, 95% CI: 0.5 to 6.8, P<0.05; Figure 3D).

In separate analyses of patients with ≥15 lymph nodes retrieved and examined (Table S2), the TO group reported potentially worse social function (MD =4, 95% CI: 0 to 8, P=0.02) and potentially more financial impact (MD =−5, 95% CI: −9 to −1, P=0.02), compared with the non-TO group.

TO and survival

The median follow-up was 60 months (IQR, 57–62 months) for patients with TO and 62 months (IQR, 60–65 months) for patients without. The median OS and median DFS were not reached in either the TO or non-TO group at the time of data cutoff. The Kaplan-Meier curves demonstrated no statistically significant differences in OS or DFS between the two patient groups (log-rank P=0.06 for OS; P=0.08 for DFS; Figure 4). However, in order to explore the early differences, we conducted additional analyses. The Breslow test revealed a transient advantage in both OS and DFS for the TO group over the non-TO group during the early follow-up period (P=0.04 for OS; P=0.045 for DFS; Table S3; Figure 4). Landmark analysis further elucidated that within the first 60 months of follow-up, the TO group exhibited significantly superior OS [68.8% vs. 59.3%, hazard ratio (HR) 0.59, 95% CI: 0.40 to 0.87, P=0.01; Table S3; Figure 5A] and DFS (62.9% vs. 55.6%, HR 0.64, 95% CI: 0.45 to 0.93, P=0.02; Table S3; Figure 5B) compared to the non-TO group. Beyond 60 months, however, the survival curves for OS and DFS converged with no discernible difference between the groups (P>0.99), and the statistical model failed to converge.

Figure 4 Kaplan-Meier analysis between the TO and non-TO groups. TO, textbook outcome.

Figure 5 Landmark analysis between TO and non-TO groups before and after 60 months of follow-up. CI, confidence interval; HR, hazard ratio; TO, textbook outcome.

Discussion

The concept of TO focuses not only on technical success but also on patient-centered management throughout the integration of innovative care models. This study found that in patients with ESCC who underwent minimally invasive McKeown esophagectomy, achieving TO was associated with improvements in short-term OS and DFS rates, as well as alleviation of dysphagia symptoms. However, it may be accompanied by a short-term decline in social function and economic burden.

This study found that the rate of achieving TO (31.9%) was consistent with previously reported rates of 24–45% (6,14,23-28). We found that serious complications (anastomotic leakage and other complications of CD III +) were the biggest obstacle to reaching TO in previous large cohort studies of TO of esophageal cancer (11,13,14,26,29,30). However, TO achievement appeared to be associated with the absence of neoadjuvant therapy, which contrasts with previous studies suggesting that neoadjuvant treatment improves TO rates (26). A possible explanation is that neoadjuvant therapy, often administered as standard care for locally advanced tumors, may induce tumor regression reducing the lymph node yield and ultimately reduce the likelihood of achieving TO (31). This finding does not challenge the value of neoadjuvant therapy but underscores the need for more meticulous perioperative management in these patients to optimize short-term outcomes.

Although the OS and DFS benefit for TO patients did reach marginal significance in long-term follow-up (log-rank P=0.06/0.08, the TO group demonstrated a significant survival advantage within 60 months post-surgery, with higher OS (68.8% vs. 59.3%; HR 0.59, P=0.01) and DFS (62.9% vs. 55.6%; HR 0.64, P=0.02) compared to the non-TO group. Achieving TO may contribute to improved survival by optimizing perioperative care and effectively mitigating early recurrence risks.

Currently, there are no reports addressing the correlation between the concept of TO in esophagectomy and patient-reported outcomes. However, considering the lymphadenectomy intensity, we noted a report has demonstrated that extensive lymphadenectomy might not decrease the HRQL of patients in esophageal cancer, but it did not observe the QOL at multiple sites through 6 months (32). Patients who achieved TO reported potentially worse social function (MD <10, P<0.05) at 7 days postoperatively and persistently greater financial difficulties throughout follow-up (baseline, 7 days, and 90 days). This contradicts intuition, as TO is designed to cover efficiency indicators such as avoiding major complications and shortening hospital stays, which should lead to a reduction in direct medical expenditures. However, this obvious contradiction precisely highlights the crucial difference between the objective treatment costs and the patients’ subjective perception of the economic burden. This counterintuitive result may be attributed to the fact that TO patients, experiencing a smoother recovery, resumed social roles earlier and thus became more acutely aware of the associated pressures (33-35). Contributing factors could include patients’ insufficient knowledge to manage complex post-discharge conditions and cope with unexpected events, as well as limited understanding of the recovery process and individual variability, which may heighten anxiety. In contrast, patients who did not receive TO treatment might have a slower recovery process, which could cause their current attention to mainly focus on physical discomfort and complex medical management. This might delay or reduce their perception and reporting of social and financial issues (36). Therefore, the financial impacts observed in the TO group may reflect a more acute and direct perception of the comprehensive economic burden of cancer treatment, rather than higher objective costs. This finding emphasizes that successful technology and perioperative outcomes do not necessarily imply a recovery in socio-economic status. TO patients exhibited potential (P<0.05, but MD <10) and sustained improvement in taste disturbance from day 7 to day 90, strongly suggesting that an uncomplicated surgical outcome—reflected by TO—may better preserve nerves or tissues related to taste, thereby improving QOL. A particularly striking finding was the clinically meaningful and substantial improvement in swallowing difficulty at 30 days post-surgery in the TO group (MD =15.1). This result stands out despite the lack of significance in the overall mixed-model analysis, indicating that TO provides crucial short-term functional advantages. This marked benefit may offset the early negative perceptions regarding social and financial domains. The potential risks to QOL highlight that technical success does not equate to holistic recovery from the patient’s perspective. Therefore, we propose incorporating QOL metrics into the standards for TO to comprehensively enhance postoperative recovery.

Enhanced nursing care for patients with complications following esophagectomy may have played a role in narrowing the QOL gap between those who did not achieve TO and those who did (37,38). Thus, although the clinical differences in the improvement of postoperative taste problems and dysphagia are limited, TO still has great potential to improve the QOL if the diagnosis and treatment process and postoperative care are further optimized.

There are methodological strengths in this study, including the use of patient data derived from a prospective database, longitudinal analyses of overall trends and intergroup variations, a large sample size, and the application of mixed-effects models to address missing data. However, limitations exist, such as its non-randomized controlled trial design, which may introduce selection bias. Furthermore, the single-center database may limit the generalizability of the results. We plan to incorporate these optimizing factors into future research.

Conclusions

In patients with ESCC who underwent minimally invasive McKeown esophagectomy, achieving TO was hindered mainly by postoperative complications, and was associated with improvements in OS, DFS and dysphagia symptoms, and also with a risk of short-term decline in QOL. Patients who achieved TO need further optimization of the treatment process and postoperative care to release the potential to improve the QOL of esophageal cancer patients after surgery.

Acknowledgments

The authors would like to thank the nursing team for their initial contribution to the esophageal cancer database in the process of data collection. This research was accepted as poster discussion of the 33nd meeting of European Society of Thoracic surgeons in 2025.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1839/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1839/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1839/prf

Funding: This work was supported by grants from the National Natural Science Foundation of China (No. 82472663), the International Cooperation Projects of the Science and Technology Department of Sichuan Province (No. 2024YFHZ0322), the Sichuan Key Research and Development Project from the Science and Technology Department of Sichuan Province (Nos. 2023YFS0044 and 2023YFQ0056), the Chengdu Science and Technology Bureau Key Research Project (No. 2024-YF05-00797-SN), the Wu Jieping Clinical Research Projects (No. 320.6750.2023-05-141), and the Sichuan Province Clinical Key Specialty Construction Project [No. (2022)70]. The funding was used to support data collection, the statistical analysis, and the cost of publishing articles.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1839/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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. The study was authorized by the Ethics Committee of the Medical Research and New Medical Technology of Sichuan Cancer Hospital & Institute (No. SCCHEC-02-2023-090) and informed consent was taken from all the patients. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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