Prognostic impact of mucinous adenocarcinoma after curative surgery for stage I–III colorectal cancer: a large population-based cohort study

Introduction

Colorectal cancer (CRC) is one of the leading causes of cancer-related deaths worldwide (1). Mucinous adenocarcinoma (MA) is a distinct subtype characterized by abundant mucin component, accounting for at least 50% of the tumor volume (2). Epidemiological data show that MA accounts for approximately 10–20% of CRC cases, with a relatively lower proportion in Asian populations and a higher proportion in Western countries (2,3). In terms of clinicopathological features, MA is more common in the proximal colon than in the rectum or distal colon (4). In addition, MA is often diagnosed at a later stage of the disease and shows a higher tendency for lymph node invasion and a risk of peritoneal metastasis compared to conventional adenocarcinoma (AC) (2-4).

However, the prognostic implication of MA as compared to AC is still inconsistent across reports due to its relatively low incidence. Many studies have shown that MA is more aggressive than AC and is considered an unfavorable subtype (5-7). In addition, MA has a lower response to existing chemotherapy than AC due to its unique histological features, which limits the therapy benefit (8-10). However, other studies have not revealed significant differences in mortality in patients with MA (11,12). In addition, the prognostic difference between MA and AC has been reported to be associated with the location and stage of tumor (13-15). However, most retrospective studies included only a limited number of patients, limiting the evidence’s strength. Meanwhile, the clinical guidelines for CRC have not clearly distinguished the treatment standards for MA and AC. With the development of multidisciplinary comprehensive treatment model, individualized treatment strategies for different patients are becoming increasingly important to improve survival outcomes (16). Therefore, accurate assessment of the impact of MA on the prognosis of patients is of great significance in guiding clinical practice. However, there is still a lack of studies based on large-scale populations that systematically analyze the prognostic value of MA in the context of modern treatment.

Therefore, this study aims to clarify the independent prognostic value of MA in the contemporary treatment model through large-sample analysis, in order to provide more evidence for risk stratification and treatment decision-making for MA patients. We present this article in accordance with the STROBE reporting checklist (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0334/rc).

Methods

Study participants

Based on data obtained from the Surveillance, Epidemiology, and End Results (SEER) Program (17 registries, Nov 2024 Sub, covering 2010–2022), patients with primary CRC diagnosed between 2010 and 2022 were initially identified. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study cohort was further restricted to individuals who had undergone curative resection and were pathologically staged as I–III. Exclusion criteria included: stage IV or unknown stage, pathological types other than AC or MA, did not receive curative resection, insufficient chemotherapy information, and unknown other information. The complete selection workflow is depicted in Figure 1.

Figure 1 Flowchart of study cohort selection. AC, adenocarcinoma; CRC, colorectal cancer; MA, mucinous adenocarcinoma.

Data collection

The following clinicopathological variables were collected for each patient: age at diagnosis (<70 vs. ≥70 years), sex (male vs. female), race (White, Black, or others), marital status (married vs. single), median household income (<$80,000 vs. ≥$80,000), preoperative carcinoembryonic antigen (CEA) level (negative vs. positive), primary tumor site (right-colon, left-colon or rectal), tumor size (<5 vs. ≥5 cm), perineural invasion (yes vs. no), number of lymph nodes resected (LN) (<12 vs. ≥12), tumor grade (I, II, III, or IV), pathological type (AC vs. MA), T stage (T1, T2, T3, or T4), N stage (N0, N1, or N2), and chemotherapy status (no chemotherapy, preoperative only, postoperative only, or both preoperative and postoperative).

Right-sided colon cancer included the cecum (C18.0), ascending colon (C18.2), hepatic flexure (C18.3), and transverse colon (C18.4). Left-sided colon cancer included the splenic flexure (C18.5), descending colon (C18.6), and sigmoid colon (C18.7).

The primary outcome of this study was overall survival (OS), and the secondary outcome was cancer-specific survival (CSS). OS was defined as the time interval from the date of curative surgery to the date of death from any cause. CSS was defined as the time interval from the date of curative surgery to the date of death attributed to CRC.

Statistical analyses

All statistical analyses were performed using R software (version 4.5.1). Data management and transformation were conducted with the dplyr (version 1.1.4) and tidyverse (version 2.0.0) packages. Between-group comparisons for categorical variables were performed using Pearson’s Chi-squared test. Survival probabilities were estimated using the Kaplan-Meier method, with between-group differences assessed by the log-rank test. Prognostic factors were identified through Cox proportional hazards regression models. Subgroup analyses were stratified by pathological stage and primary tumor site. To minimize confounding, propensity score matching (PSM) was performed using the MatchIt package (version 4.7.2). P value <0.05 was considered statistically significant.

Results

Patients’ characteristic

Between 2010 and 2022, a total of 69,335 patients with stage I–III CRC who underwent curative surgery were identified from the database. The final cohort comprised 63,737 patients with AC and 5,598 patients with MA. Table 1 summarizes the clinicopathological characteristics of the two groups.

Relative to the AC group, patients in the MA group were significantly older (≥70 years: 50.8% vs. 42.9%, P<0.001) and more frequently female (51.4% vs. 47.6%, P<0.001. Furthermore, the MA group exhibited distinct tumor biological behaviors and more aggressive features, including a higher rate of preoperative CEA positivity (45.2% vs. 36.2%, P<0.001), a predominant colon location (90.3% vs. 82.6%, P<0.001), larger tumor size (≥5 cm: 52.0% vs. 31.9%, P<0.001), and a higher proportion of poor differentiation (grade III–IV: 20.2% vs. 16.6%, P<0.001). Regarding pathological stage, the MA group presented with more locally advanced disease, characterized by a higher percentage of T4 stage (20.5% vs. 13.1%, P<0.001) and N2 stage (16.4% vs. 13.1%, P<0.001). Notably, although the proportion of patients receiving chemotherapy was similar (MA: 40.7% vs. AC: 41.5%).

Prognostic impact of MA in stage I–III CRC

The median follow-up time for the entire cohort was 84 months. The Kaplan-Meier survival curves for the overall CRC cohort are presented in Figure 2. In the overall cohort, patients with MA had significantly worse survival outcomes compared to those with AC. The 5-year OS rate was 63.9% for the MA group versus 71% for the AC group (P<0.001, Figure 2A). Similarly, the 5-year CSS rate was significantly lower in the MA group (76.9% vs. 82.3%, P<0.001, Figure 2B). To investigate whether the prognostic impact of MA across disease stages, we performed stage-stratified Kaplan-Meier analyses. This survival disadvantage exhibited a clear stage-dependent gradient (Figure 2C-2H), being most obvious in stage III disease (P<0.001 for both OS and CSS, Figure 2G,2H).

Figure 2 Kaplan-Meier curves for survival outcomes between the AC and MA groups were compared in overall CRC cohort and stage I–III subgroups. (A) Overall survival in the overall cohort. (B) Cancer-specific survival in the overall cohort. (C) Overall survival in stage I patients. (D) Cancer-specific survival in stage I patients. (E) Overall survival in stage II patients. (F) Cancer-specific survival in stage II patients. (G) Overall survival in stage III patients. (H) Cancer-specific survival in stage III patients. AC, adenocarcinoma; CRC, colorectal cancer; MA, mucinous adenocarcinoma.

We then performed a subgroup analysis by tumor site, and the results showed consistency with the primary analysis. Notably, the previously observed stage-dependent pattern persisted (Figures S1,S2). The survival disadvantage of MA relative to AC became progressively more pronounced with advancing pathological stage, with the most significant differences consistently observed in stage III disease for both tumor site (all P<0.001; Figure S1G,S1H and Figure S2G,S2H).

However, cox proportional hazards regression analyses confirmed that the independent adverse prognostic impact of mucinous histology was confined to stage III disease. In both colon and rectal cancer subgroups, MA histology did not demonstrate independent prognostic value for OS or CSS in stage I or stage II disease following multivariate adjustment (all P>0.05; Tables S1-S4). Conversely, for patients with stage III disease, MA remained a significant independent predictor of worse survival outcomes in both colon (adjusted HR for OS =1.12, for CSS =1.16; all P<0.001; Table S5) and rectal cancer (adjusted HR or OS =1.17, for CSS =1.26; all P<0.05; Table S6). Detailed results of these regression analyses are provided in Tables S1-S6.

Prognostic impact of MA stratified by chemotherapy modality in stage III disease

Considering the consistently independent prognostic significance of MA in stage III colon and rectal cancer, we investigated if this effect was affected by the chemotherapy modality.

Among stage III colon cancer patients who did not receive chemotherapy, MA was not an independent risk factor (all P>0.05; Figure S3A,S3B). In contrast, the adverse prognostic impact of MA was significant among patients who received postoperative chemotherapy (all P<0.001; Figure S3C,S3D). In this subgroup, MA was an independent risk factor for both worse OS (HR =1.21, 95% CI: 1.11–1.31, P<0.001) and CSS (HR =1.29, 95% CI: 1.17–1.42, P<0.001) (Table S7).

In stage III rectal cancer, a similar pattern was observed. Among patients who did not receive chemotherapy, no significant survival difference was observed between MA and AC groups (OS P=0.46, CSS P=0.916, Figure S4A,S4B). Kaplan-Meier analyses observed that MA was associated with poorer survival outcomes in patients receiving chemotherapy compared to AC (Figure S4C-S4H). Notably, the sequential administration of both preoperative and postoperative chemotherapy appeared to narrow the survival gap between MA and AC groups, reducing the adverse prognostic impact of MA (Figure S4G,S4H). Compared with either preoperative chemotherapy alone or postoperative chemotherapy alone in rectal cancer, patients with MA have greater survival benefits from the combined preoperative and postoperative chemotherapy than AC (Figure S4C-S4H). Multivariate analyses within distinct chemotherapy subgroups revealed that MA was an independent predictor of worse survival in the preoperative chemotherapy cohort (OS: HR =1.37, 95% CI: 1.05–1.79, P=0.02; CSS: HR =1.58, 95% CI: 1.17–2.12, P=0.003) (Table S8) and in the postoperative chemotherapy cohort (OS: HR =1.47, 95% CI: 1.07–2.03, P=0.02; CSS: HR =1.53, 95% CI: 1.06–2.21, P=0.02) (Table S9). However, in the combined preoperative and postoperative chemotherapy cohort, MA was not an independent prognostic factor in the final multivariate models (OS: HR =1.32, 95% CI: 0.96–1.81, P=0.08; CSS: HR =1.24, 95% CI: 0.87–1.78, P=0.24) (Table 2).

Prognostic impact of MA after PSM in stage III disease

To minimize potential confounding, PSM was performed to stage III colon and rectal cancer patients stratified by chemotherapy modality. After PSM, the clinicopathological characteristics of the groups were well-balanced, with no significant differences found across all variables (Table S10 and Table 3, all P>0.05).

For stage III colon cancer, after PSM, the adverse prognostic impact of MA was confined to the subgroup receiving postoperative chemotherapy (Figure 3A-3D). In this matched cohort, MA was a significant independent risk factor for both worse OS (HR =1.21, 95% CI: 1.11–1.31, P<0.001) and CSS (HR =1.29, 95% CI: 1.17–1.42, P<0.001) (Table S11). For stage III rectal cancer, PSM analysis revealed a nuanced pattern (Figure 4A-4H). In the matched cohort receiving preoperative chemotherapy only, MA was associated with worse OS (HR =1.37, 95% CI: 1.04–1.82, P=0.03) and CSS (HR =1.59, 95% CI: 1.17–2.18, P=0.003) (Table S12). Similarly, in the matched cohort receiving postoperative chemotherapy only, MA predicted poorer OS (HR =1.45, 95% CI: 1.04–2.02, P=0.03) and CSS (HR =1.50, 95% CI: 1.02–2.19, P=0.04) (Table S13). However, in the matched cohort receiving combined preoperative and postoperative chemotherapy, no statistically significant differences in 5-year OS or CSS were observed between the MA and AC groups (OS P=0.27, CSS P=0.52; Figure 4G,4H). MA was not an independent prognostic factor in the preoperative and postoperative chemotherapy group (OS: HR =1.21, 95% CI: 0.86–1.69; CSS: HR =1.14, 95% CI: 0.77–1.67) (Table 4).

Figure 3 Kaplan-Meier curves after PSM for survival outcomes between the AC and MA groups were compared in stage III colon cancer cohort based on different chemotherapy modalities. (A) Overall survival in the No chemotherapy group. (B) Cancer-specific survival in the No chemotherapy group. (C) Overall survival in the postoperative chemotherapy group. (D) Cancer-specific survival in the postoperative chemotherapy group. AC, adenocarcinoma; MA, mucinous adenocarcinoma; PSM, propensity score matching.

Figure 4 Kaplan-Meier curves after PSM for survival outcomes between the AC and MA groups were compared in stage III rectal cancer cohort based on different chemotherapy modality. (A) Overall survival in the No chemotherapy group. (B) Cancer-specific survival in the No chemotherapy group. (C) Overall survival in the preoperative chemotherapy group. (D) Cancer-specific survival in the preoperative chemotherapy group. (E) Overall survival in the postoperative chemotherapy group. (F) Cancer-specific survival in the postoperative chemotherapy group. (G) Overall survival in the preoperative and postoperative chemotherapy group. (H) Cancer-specific survival in the preoperative and postoperative chemotherapy group. AC, adenocarcinoma; MA, mucinous adenocarcinoma; PSM, propensity score matching.

Discussion

The results of our large retrospective study provide valuable insights into the prognostic role of MA in the context of modern, stage-adapted treatment for CRC. Our principal finding is that while MA is an independent adverse prognostic factor in stage III disease, its prognostic significance is critically modified by chemotherapy modality. Specifically, the survival disadvantage of MA was most evident in patients receiving single-modality chemotherapy but disappeared among stage III rectal cancer patients treated with intensive combined preoperative and postoperative chemotherapy.

In contemporary clinical practice, the individualized treatment is usually guided by high-risk factors, including histological characteristics and genetic features (17-19). As a unique histological subtype of CRC, MA differs significantly from AC (2,3). Currently, the studies present conflicting results about the prognosis and survival of patients with MA (5,8,11,12,20-22). It is essential to investigate the prognostic implications by larger population data of this specific subtype of MA to provide more effective treatment to patients. Through detailed stage-stratified and treatment-stratified analyses, our study found that the unfavorable prognosis usually associated with MA is not a unique characteristic but is significantly influenced by disease stage and chemotherapy modality. In stages I and II disease, after adjusting for other clinicopathological factors, MA was not an independent prognostic factor for survival outcomes. This suggests that MA exhibits a biological behavior that is not more aggressive than that of AC when treated with curative surgery alone. Consequently, when evaluating prognosis and making treatment decisions, greater emphasis should be placed on established high-risk factors such as depth of invasion and lymphovascular invasion, rather than concentrating solely on the histological type of MA in stage I–II disease.

Our study indicates a substantial relationship between tumor histology and the effectiveness of chemotherapy. For stage III disease, chemotherapy serves as a crucial treatment designed to eliminate micro-metastatic disease and enhance survival outcomes (23,24). However, our data indicate that the survival benefit derived from such chemotherapy appears substantially lower for patients with MA than for those with AC. This suggests that MA exhibits a state of relative chemotherapy resistance, resulting in diminished treatment benefit compared to AC, which is consistent with the findings of the majority of current studies (8-10,25). Crucially, this resistance appears not to be absolute. In the subset of stage III rectal cancer patients who received the stronger regimen—combined preoperative and postoperative chemotherapy—the prognostic disadvantage of MA was eliminated. The resistance of MA to chemotherapy is attributed to multiple biological factors. The prevalence of extracellular mucin in MA may serve as a biochemical and physical barrier that limits the distribution and penetration of drugs into tumor cells (2). Furthermore, MA is molecularly distinct, with a higher prevalence of microsatellite instability (MSI) and BRAF mutations—alterations known to influence the response to chemotherapy (25-27). The observation that intensified chemotherapy appears to mitigate the MA-associated risk supports the hypothesis that overcoming this biological barrier requires a more robust therapeutic approach, potentially through higher cumulative drug exposure of chemotherapy administration (11,28). This crucial result implies enhancing treatment intensity may overcome the biological barriers that limit standard chemotherapy efficacy in stage III mucinous colon AC (29-32). The question of whether chemotherapy administration should be routinely intensified or complemented with novel agents for stage III colon MA warrants investigation in prospective trials. Additionally, the role of high-quality preoperative diagnosis in identifying the mucinous phenotype early, thereby potentially altering the therapeutic pathway toward more intensive therapy strategies, should be emphasized (33).

This study provides strong evidence for the prognosis and response to chemotherapy of colorectal MA based on a large real-world population data. However, this study also has several limitations. First, due to the inherent nature of the SEER database, several important clinical and pathological covariates were unavailable for analysis. Specifically, for patients with rectal cancer, information on mesorectal fascia involvement, extramural vascular invasion (EMVI), and detailed radiotherapy parameters (including radiotherapy dose and regimen) was not available in the SEER database. These variables are well-established prognostic factors that may influence both recurrence-free survival and OS in rectal cancer patients. The absence of such information may introduce residual confounding and bias. Second, the lack of detailed information on specific chemotherapy regimens, treatment cycles, reasons for not administering adjuvant chemotherapy, and patient performance status may lead to residual confounding and bias. Third, although PSM helps balance measured covariates between groups, it cannot adjust for unmeasured factors that may affect both treatment allocation and clinical outcomes. Fourth, the lack of molecular data (e.g., MSI, RAS/BRAF status) prevents a deeper exploration of the observed chemotherapy interaction. Nevertheless, this study systematically elucidates the prognostic characteristics of MA based on different stages and chemotherapy regimens and provides important evidence for future research development and the formulation of individualized treatments.

Conclusions

Our study provides supporting evidence from a large-scale cohort for the distinct prognostic role of MA in CRC. Our principal finding is that MA is an independent adverse prognostic factor in stage III disease when patients are receiving single-modality chemotherapy. However, among stage III rectal cancer patients treated with combined preoperative and postoperative chemotherapy, the prognostic disadvantage of MA was eliminated.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0334/rc

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0334/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0334/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 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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