Postoperative frailty among elderly patients undergoing radical surgery for gastrointestinal tumors and its relationship with prognosis

Introduction

Population aging is accelerating worldwide, and the incidence of malignancies increases markedly with age (1-3). In China, new cancer cases and deaths account for 23.7% and 30.2% of the global burden, respectively, ranking at an upper-middle level among 185 countries or regions, with gastrointestinal cancers such as esophageal, gastric, liver, and colorectal cancers contributing to nearly half of the global incidence and mortality rates (4). Gastrointestinal tumors are not only the most common malignancies in China but also a major global health threat (5). According to national cancer registry data, gastric and colorectal cancers rank second and third, accounting for 10.25% and 9.87% of all cancer cases (6,7). With advances in medical technology, the number of elderly patients undergoing surgical treatment has increased substantially. Surgical resection remains the primary treatment for gastrointestinal tumors and can improve survival and quality of life (6).

Compared with younger patients, elderly individuals have reduced physiological reserve, limited compensatory capacity, and common comorbidities such as hypertension, diabetes, coronary artery disease, and chronic pulmonary disease, which lower surgical tolerance and increase perioperative risk (8). Frailty is a common but potentially reversible geriatric syndrome. It is characterized by reduced physiological reserve and resilience and is strongly associated with adverse outcomes (9). Frail patients often present with fatigue, unexplained weight loss, reduced activity tolerance, recurrent infections, appetite loss, cognitive impairment, and muscle weakness (10). Its mechanisms involve chronic inflammation, endocrine dysregulation, and cellular aging. Although there is no uniform diagnostic standard, more than 60 assessment tools have been developed, and the prevalence of frailty in surgical populations has been reported as 18.6–56% (11).

Accumulating evidence shows that frailty is closely associated with higher postoperative complications, prolonged hospital stay, functional decline, and increased mortality (12). Therefore, the American expert consensus in 2012 and the Chinese Geriatrics Society consensus in 2016 and 2022 recommended routine preoperative frailty assessment to guide perioperative management and improve outcomes (13). Nevertheless, most studies have focused on preoperative frailty, overlooking its dynamic and perioperative nature (11). Frailty may progress or be triggered by surgical stress, which disrupts homeostasis and predisposes elderly patients to frailty or disability, thereby increasing complications and worsening prognosis (14,15). Our previous study demonstrated that preoperative frailty was strongly associated with higher postoperative complication rates, increased severity, and poor recovery, and together with advanced age, severe comorbidities, and prolonged operative time, constituted the core determinants of poor outcomes (8).

Based on these findings, this study aimed to systematically investigate postoperative frailty (PF) in elderly patients with gastrointestinal cancer, focusing on its incidence, risk factors, complications, short-term outcomes, and long-term prognosis, to provide evidence for its clinical recognition and management. We present this article in accordance with the STARD reporting checklist (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-aw-938/rc).

Methods

Study population

This retrospective study was approved by the First Affiliated Hospital of Anhui Medical University (No. PJ 2025-10-40), and all participants provided written informed consent. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Elderly patients undergoing elective radical resection of gastrointestinal tumors under general anesthesia were retrospectively analyzed. In total, 398 patients were analyzed, including 183 non-frail and 215 frail cases postoperatively.

Inclusion criteria

Patients were eligible if they were aged ≥60 years, had an American Society of Anesthesiologists (ASA) physical status of class I–IV, and possessed complete clinical records.

Exclusion criteria

Patients were excluded if they required emergency surgery, if intraoperative exploration revealed tumor metastasis necessitating palliative rather than curative resection, or if clinical records were incomplete or follow-up data were unavailable.

Frailty assessment

Frailty was evaluated using the Edmonton Frail Scale (EFS), a validated tool for rapid screening in outpatient and inpatient populations. The EFS includes 11 items across 9 domains: cognition (clock-drawing, 2 points), general health status (hospitalizations in the past year, 2 points; self-rated health, 2 points), functional independence (instrumental activities of daily living, 2 points), social support (availability of assistance, 2 points), medication use (polypharmacy, ≥5 prescription drugs, 1 point; nonadherence, 1 point), nutrition (weight loss, 1 point), mood (depression, 1 point), continence (1 point), and functional performance [timed up-and-go (TUG), 2 points]. Scores range from 0 to 17, with higher scores indicating greater frailty. The English version of the EFS has demonstrated acceptable reliability (Cronbach’s α=0.62; κ=0.77). Frailty was categorized as non-frail (≤5 points), pre-frail (6–7 points), and frail (8–17 points). For the primary analysis, PF was defined using the EFS assessed on postoperative day (POD) 5; patients with EFS ≥8 were classified as frail, whereas those with EFS ≤7 (including non-frail and pre-frail) were classified as non-frail. The EFS was administered preoperatively and on POD 5. Preoperative EFS was additionally incorporated as a baseline covariate in multivariable models to account for baseline frailty status.

Pathology classification

Pathological staging was determined according to the tumor-node-metastasis (TNM) classification of the International Union Against Cancer (UICC) Atlas of TNM Staging, and defined as follows: Stage I, lesions confined to the gastrointestinal tract; Stage II, involvement of the surrounding peritoneal cavity without extension to other organs; Stage III, invasion of adjacent organs or tissues; and Stage IV, presence of distant metastasis with extra-nodal organ involvement.

Charlson Comorbidity Index (CCI)

The CCI, developed in 1987 and updated in 2008, consists of three domains: disease assessment, severity weighting, and cumulative scoring. It covers 23 disease categories, each assigned 1, 2, 3, or 6 points based on severity. For patients aged ≥50 years, scores are adjusted upward, with 1 point for ages 50–59 years and an additional point for each subsequent decade. Higher scores indicate greater comorbidity burden, classified as mild [2–3], moderate [4–6], or severe [≥7]. In this study, all participants were ≥60 years, giving a baseline age-adjusted score of 2. Because all cases involved malignancy (2 points), the minimum CCI score was 4, placing every patient in at least the moderate comorbidity category.

Postoperative complications

Postoperative complications were assessed according to the Expert Consensus on the Registration Criteria for Postoperative Complications in Gastrointestinal Surgery in China. This consensus provides standardized definitions and grading of gastrointestinal, wound-related, respiratory, cardiovascular, urinary, infectious, thromboembolic, and other complications. In this study, overall postoperative complications were defined as the occurrence of ≥1 complication within these categories during the first month after surgery.

Statistical analysis

The data were shown as n (percentage). The comparisons of data between the two groups were performed using Fisher’s exact test or the Chi-squared test. To identify factors associated with PF, we further performed univariable and multivariable logistic regression analyses and reported odds ratios (ORs) with 95% confidence intervals (CIs). Covariates in the multivariable model were prespecified based on clinical relevance within a “preoperative status-intraoperative intervention-postoperative outcome” framework, rather than selected solely by univariable significance. Given the correlation between preoperative and postoperative EFS, preoperative EFS was included as a baseline covariate; multicollinearity was assessed using variance inflation factors (VIFs; all VIF <1.5). In the multivariable logistic regression model, PF status was the dependent variable, and age ≥70 years, TNM stage III–IV, severe CCI, open surgery, preoperative frailty, abnormal preoperative albumin, and operative time ≥240 min were included as independent variables. In addition, we conducted a subgroup analysis restricted to patients who were non-frail preoperatively. Long-term survival outcomes (overall survival and disease-free survival) were analyzed using Cox proportional hazards regression models, with survival time as the dependent variable and PF status plus the covariates above as independent variables; the proportional hazards assumption was assessed using Schoenfeld residuals (P>0.05). P values less than 0.05 were considered statistically significant.

Results

Univariate analysis of clinicopathology and PF or non-postoperative frailty (NPF) among elderly patients who underwent radical surgery for gastrointestinal tumors

This analysis aimed to identify clinicopathological factors associated with PF in elderly patients undergoing radical gastrointestinal tumors resection. Patients with PF were elderly, with 61.9% aged 70–79 years compared with 47.5% in the non-frail group (P=0.003, Table 1). They also had a higher prevalence of severe comorbidity (51.2% vs. 35.5%, P=0.002) and more frequent hypoalbuminemia (64.2% vs. 49.7%, P=0.004) (Table 1). Intraoperative and surgical features also differed, with PF patients more often undergoing open surgery (44.2% vs. 31.7%, P=0.01), experiencing greater blood loss ≥150 mL (38.1% vs. 23.0%, P=0.001), and having longer operation times ≥240 min (52.1% vs. 37.2%, P=0.003) (Table 1). Preoperative frailty was the most striking association (30.7% vs. 3.8%, P<0.001). Collectively, these findings suggest that advanced age, severe comorbidity, impaired nutritional status, and adverse intraoperative parameters were associated factors to PF in this patient population.

Multivariate logistic analysis of clinicopathological factors for PF among elderly patients who underwent radical surgery for gastrointestinal tumors

To evaluate factors associated of PF, multivariate logistic regression was performed (Table 2). Age ≥70 years (OR =1.214; 95% CI: 1.085–1.392), TNM stage III–IV (OR =1.196; 95% CI: 1.033–1.417), severe comorbidity (OR =1.243; 95% CI: 1.117–1.409), open surgery (OR =1.185; 95% CI: 1.056–1.680), preoperative frailty (OR =1.647; 95% CI: 1.284–2.305), hypoalbuminemia (OR =1.302; 95% CI: 1.106–1.553), and operative time ≥240 min (OR =1.157; 95% CI: 1.113–1.328) were all significant factors associated with PF. These results suggest that that advanced age, greater tumor burden, severe comorbidity, invasive surgical approach, impaired nutritional status, and prolonged operative stress collectively predisposed elderly patients to PF.

Comparisons of postoperative complications between patients with PF or NPF among elderly patients who underwent radical surgery for gastrointestinal tumors

To examine the impact of PF on surgical outcomes, we compared the incidence of complications between PF and NPF patients (Table 3). Overall, postoperative complications occurred in 45.1% of PF patients compared with 22.4% of NPF patients (P<0.001). Specific complications with significant differences included intestinal obstruction (12.6% vs. 6.0%, P=0.03), pleural effusion (2.8% vs. 0.0%, P=0.03), pulmonary infection (15.3% vs. 7.6%, P=0.02), and acute kidney injury (8.8% vs. 3.3%, P=0.02). These findings indicate that PF was strongly associated with a higher incidence of overall and system-specific complications following radical gastrointestinal tumors surgery in elderly patients.

Predictive value of PF for complications

To evaluate the association between PF and complications, as well as the predictive value of frailty assessment, we performed comparative and receiver operating characteristic (ROC) analyses (Figure 1). Postoperative complications occurred in 45.1% of PF patients (97/215) compared with 22.4% of non-frail patients (41/183), a highly significant difference (P<0.001, Figure 1A). It also showed that the EFS score at POD 5 demonstrated good discrimination for overall complications, with an area under the curve (AUC) of 0.83 (P<0.001), sensitivity of 61.6%, and specificity of 86.5% at a cutoff of 7 (Figure 1B). Additionally, a sensitivity analysis was performed by excluding patients who were diagnosed with complications within the first 5 PODs (n=14). ROC analysis indicated that the POD 5 EFS predicted subsequent complications within 1 month (AUC, 0.84; 95% CI: 0.80–0.88; P<0.001), consistent with the original estimate (AUC, 0.83). Collectively, these findings indicate that PF was strongly associated with a higher incidence of complications and that early postoperative EFS assessment may help identify patients at higher risk.

Figure 1 Predictive value of PF for complications. (A) Comparisons of total postoperative complications between patients with PF (n=215) or not (NPF, n=183) among elderly patients who underwent radical surgery for gastrointestinal tumors. The comparisons of data between the two groups were done by Fisher’s exact test. (B) ROC analysis of the predictive value of the EFS at 5 days post-operation for total postoperative complications in elderly patients who underwent radical surgery for gastrointestinal tumors. AUC, area under the curve; EFS, Edmonton Frail Scale; NPF, non-postoperative frailty; PF, postoperative frailty; ROC, receiver operating characteristic.

Comparisons of short-term prognosis between patients with PF or NPF among elderly patients who underwent radical surgery for gastrointestinal tumors

To assess the impact of PF on short-term outcomes, prognostic indicators were compared between frail and non-frail patients (Table 4). In-hospital mortality was higher in the PF group than in the NPF group (3.7% vs. 0.5%, P=0.042). Similarly, postoperative intensive care unit (ICU) readmission occurred more frequently in PF patients (7.0% vs. 2.2%, P=0.03), as did unplanned readmission within 30 days after discharge (7.4% vs. 1.6%, P=0.008). These findings indicate that PF was significantly associated with increased early adverse events and poorer short-term outcomes following radical gastrointestinal tumors surgery in elderly patients.

Comparisons of overall survival and disease-free survival

To evaluate the association between PF and long-term survival, Kaplan-Meier analyses were performed (Figure 2). As shown in Figure 2A, overall survival at 3 years was significantly reduced in PF patients compared with non-frail patients (P=0.002). Similarly, disease-free survival was also lower in the PF group (Figure 2B, P=0.004). These results demonstrated that PF was associated with impaired long-term survival outcomes, suggesting an association with poorer long-term outcomes in elderly patients undergoing radical gastrointestinal tumors surgery. To account for potential confounding, we further performed Cox proportional hazards models adjusting for TNM stage, age ≥70 years, overall postoperative complications, and CCI. PF remained an independent predictor of 3-year overall survival [hazard ratio (HR) =2.11, 95% CI: 1.54–2.89; P<0.001] and disease-free survival (HR =1.96, 95% CI: 1.43–2.69; P<0.001).

Figure 2 Comparisons of overall survival (A) and disease-free survival (B) between patients with PF (n=215) or not (NPF, n=183) among elderly patients who underwent radical surgery for gastrointestinal tumors. NPF, non-postoperative frailty; PF, postoperative frailty.

Discussion

This study suggests that PF is prevalent among elderly patients undergoing radical resection for gastrointestinal tumors and is closely linked to adverse clinical outcomes. Patients with PF exhibited higher incidences of postoperative complications, intensive care unit readmission, and unplanned readmission within 30 days, along with significantly reduced long-term overall and disease-free survival. Multivariate analysis further identified advanced age, higher TNM stage, severe comorbidity, open surgical approach, prolonged operative time, low preoperative albumin, and preoperative frailty as factors independently associated of PF. Collectively, these findings underscore PF as a clinically relevant marker associated with adverse outcomes in this patient population.

Our findings align closely with previous research, reinforcing frailty as a factor associated of adverse postoperative outcomes in patients with gastrointestinal tumors. Consistent evidence indicates that frailty significantly increases the risk of postoperative complications in gastric cancer, independent of tumor stage and grade (16). Similarly, a meta-analysis by Zhang et al. demonstrated that frailty more than doubled the risk of mortality (17), a result subsequently confirmed in both colorectal (18) and gastric cancer cohorts (19). Epidemiological studies further report a high prevalence of frailty in gastrointestinal cancer, with rates up to 27% (17), and more than half of elderly patients exhibiting frailty features in comprehensive geriatric assessments (20).

In contrast to previous investigations confined to static preoperative assessments, our study was the first to delineate heterogeneous PF trajectories within one year after gastric cancer surgery (21), identifying a subgroup with a distinct “poor prognosis” frailty progression pattern. This dynamic perspective provides novel evidence linking frailty to long-term functional recovery (22). Variability across studies may reflect methodological differences, as many earlier analyses employed cross-sectional or short-term follow-up designs (18,19), whereas our longitudinal approach captured the evolving nature of frailty (21). Additionally, cohort-specific factors may contribute; for example, Asian populations may exhibit unique frailty trajectories influenced by body composition and healthcare resource allocation (19). Collectively, these observations highlight the necessity of a comprehensive perioperative frailty monitoring framework (21,23). Standardized frailty assessment should be incorporated into routine preoperative evaluation, with greater emphasis on early postoperative interventions, particularly targeted rehabilitation for high-risk patients (24,25). Future studies should focus on multidisciplinary, context-specific strategies to improve outcomes in elderly patients with gastrointestinal tumors.

The adverse impact of frailty on postoperative outcomes in patients with gastrointestinal cancer arises from multiple mechanisms, including reduced physiological reserve, metabolic imbalance, and systemic inflammation. Previous studies have demonstrated that frailty is significantly associated with increased postoperative complication risk (17), possibly due to chronic low-grade inflammation and impaired protein synthesis commonly observed in frail patients. Evidence also indicates that gastric cancer patients with preoperative frailty have a markedly higher risk of heterogeneous frailty trajectories within one year after surgery (21), reflecting the sustained disruption of homeostatic regulation under surgical stress. Notably, frailty not only affects short-term outcomes but is also strongly associated with reduced long-term survival (17), potentially driven by interactions between the tumor microenvironment and systemic inflammation. Intraoperative factors such as prolonged operative time and blood loss may exacerbate vulnerability by increasing metabolic demand (18,26), while higher tumor burden may further impair immune function through persistent activation of inflammatory pathways (16). Moreover, frail patients exhibit a significantly greater incidence of grade ≥3 toxicities compared with non-frail patients (20), underscoring the role of limited metabolic reserve in reducing treatment tolerance. Importantly, long-term survival in gastrointestinal cancer partially depends on successful delivery of adjuvant chemotherapy. In our cohort, chemotherapy completion was markedly lower in patients with PF than in those without PF (42.3% vs. 76.5%; P<0.001). Mediation analysis indicated that reduced chemotherapy completion partially mediated the association between PF and 3-year survival (mediation proportion, 31.7%), supporting a pathway whereby early PF may impair treatment tolerance and completion and thereby contribute to poorer long-term outcomes. These findings highlight the importance of routine frailty assessment in gastrointestinal cancer patients (23) and provide a rationale for developing individualized perioperative management strategies tailored to frail populations.

We further assessed which EFS domains most commonly contributed to shifts in frailty status. Multimorbidity burden was the leading contributor (41.5%, 62/149), followed by worsening functional performance captured by the TUG component (28.4%, 42/149) and nutritional impairment (21.6%, 32/149); mild cognitive decline accounted for 8.5% (13/149). These findings suggest several actionable targets. First, preoperative prehabilitation over 2–4 weeks could be implemented, including oral nutritional supplementation, low-to-moderate walking and resistance training, and optimization of comorbidities. Second, intraoperative stress should be minimized by prioritizing minimally invasive approaches when feasible and reducing blood loss and operative time. Third, early postoperative multimodal care should be strengthened, with multimodal analgesia and mobilization initiated on POD 1–3 and intensified after POD 5 EFS reassessment. Finally, structured post-discharge follow-up within the first 3 months may sustain rehabilitation and nutritional recovery, and could improve tolerance and completion of adjuvant therapy.

Our findings highlight key clinical implications. Frailty, rather than chronological age, may capture vulnerability beyond chronological age and was associated with perioperative risk and long-term prognosis in gastrointestinal cancer surgery. Early PF assessment, particularly with the EFS on day 5, showed strong discrimination (AUC =0.83), suggesting potential utility in timely risk stratification and intervention. Prehabilitation measures such as nutritional support, exercise, and psychological care may enhance physiological reserve and improve both short- and long-term outcomes.

There are several limitations in this study. First, its single-center retrospective design may limit generalizability. Second, frailty was assessed only at baseline and on POD 5, without capturing longer-term trajectories. Third, important confounders such as socioeconomic status, tumor biology, adjuvant therapy, and rehabilitation adherence were not fully considered, which may have contributed to outcome heterogeneity. Early identification of high-risk patients and targeted perioperative interventions may help optimize outcomes. Future multicenter prospective studies with extended follow-up and comprehensive evaluation of biological, social, and treatment-related factors are needed to validate these findings and guide precision management in this population.

Conclusions

In conclusion, PF is a prevalent and clinically significant condition associated with prognosis in elderly patients undergoing radical gastrointestinal cancer surgery. It is associated with higher complication rates, delayed functional recovery, and diminished long-term survival. These results highlight the need for routine frailty screening, with dynamic assessment integrated across the perioperative continuum to guide risk stratification and targeted intervention.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-aw-938/rc

Data Sharing Statement: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-aw-938/dss

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-aw-938/prf

Funding: This study was supported by the Health Research Program of Anhui (No. AHWJ2024Aa40001).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-aw-938/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. This retrospective study was approved by the First Affiliated Hospital of Anhui Medical University (No. PJ 2025-10-40), and all participants provided written informed consent. The 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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