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Mucinous histology is a negative predictor of neoadjuvant chemoradiotherapy for locally advanced rectal adenocarcinoma

BMC Gastroenterology volume 24, Article number: 263 (2024) Cite this article

Abstract

Background

Neoadjuvant chemoradiotherapy (NCRT) followed by total mesorectal excision (TME) is the standard treatment for locally advanced rectal cancer (LARC). Mucinous adenocarcinoma (MAC) is a potential poor prognosis subgroup of rectal cancer. However, the predictive value of MAC in NCRT treatment of LARC is controversial.

Methods

A comprehensive literature search of PubMed, Embase, and the Cochrane Library was performed. All studies examining the effect of MAC on CRT response in LARC were included. Outcomes of MAC were compared with non-specific adenocarcinoma (AC) by using random-effects methods. Data were presented as odds ratios (ORs) with 95% confidence intervals (CIs). The main outcomes were the rates of pathological complete response (pCR), tumor and nodal down-staging, positive resection margin rate, local recurrence, and overall mortality.

Results

Fifteen studies containing comparative data on outcomes in a total of 9,238 patients receiving NCRT for LARC were eligible for inclusion. MAC had a reduced rate of pCR (OR, 0.38; 95% CI, 0.18–0.78) and tumor down-staging (OR, 0.31; 95% CI, 0.22–0.44) following NCRT compared with AC. MAC did not significantly affect nodal down-staging (OR, 0.42; 95% CI, 0.16–1.12) after NCRT.

Conclusion

MAC of LARC was found to be a negative predictor of response to NCRT with lower rates of pCR and tumor down-staging for LARC. The nodal down-staging of MAC was relatively lower than that of AC, although the differences were not statistically significant.

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Introduction

Colorectal cancer (CRC) is the third most common cancer and a major contributor to cancer-related mortality worldwide [1]. The most common histology subtype of rectal (RC) is non-specific adenocarcinoma (AC). Mucinous adenocarcinoma (MAC) of RC, characterized by the presence of more than 50% extracellular mucin in the tumor volume, ranks as the second most prevalent subtype after AC [2,3,4,5]. Clinically, locally advanced rectal cancer (LARC) occupies the majority of RC in oncologists daily work. Neoadjuvant chemoradiotherapy (NCRT) followed by total mesorectal excision (TME) has become the standard treatment for LARC [6]. NCRT aims to downstage the primary tumor, reduce the incidence of local recurrence, increase the rate of sphincter preservation, and potentially improve overall survival of LARC patients [7, 8]. However, the response to NCRT varies among patients, with the pathological complete response (pCR) rate ranging from 10–30% [9]. Thus, the potential mechanisms of the NRCT response difference of LARC need to be clarified.

MAC is often considered as a poor predictor of response to preoperative therapies including chemotherapy and radiotherapy in LARC compared to AC [10]. Several studies have also reported that rectal MAC exhibits a poor response to NCRT, resulting in inferior tumor downstaging and worse outcomes compared to AC [11,12,13]. However, a study by Hugen et al. analyzed the existing literature on rectal MAC and found no significant difference in overall survival (OS) between MAC and AC patients [14]. Consequently, there is an urgent need to resolve this controversy and identify patients who will benefit from NCRT, which could guide therapeutic decisions and potentially prompt the development of novel alternative treatments in LARC.

Because of the treatment strategies are no different between MAC and AC according to current LARC management guidelines, this meta-analysis aims to investigate whether MAC is indeed a poor indicator of response to NCRT. By systematically analyzing the available evidence, we intend to shed light on the role of MAC in NCRT of LARC and its implications for treatment outcomes. Understanding the specific characteristics and behavior of MAC in the context of NCRT will provide valuable insights into the management of LARC and contribute to the advancement of personalized treatment strategies.

Materials and methods

Literature search and study selection

According to the guidelines of the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) statement, a systematic search was conducted on PubMed, Embase, and Cochrane Library to identify relevant studies published in English, focusing on the response following preoperative neoadjuvant chemoradiotherapy (NCRT) in rectal cancer. The search algorithm included the following terms: (rectal or rectum) AND (neoadjuvant chemotherapy OR neoadjuvant chemoradiotherapy OR neoadjuvant radiotherapy OR preoperative chemotherapy OR preoperative chemoradiotherapy OR preoperative radiotherapy) AND (colloid OR mucinous OR mucin) AND (cancer OR adenocarcinoma OR carcinoma) AND (response OR outcome OR survival). The most recent search was conducted on November 09, 2021. Two authors reviewed these literatures and conducted risk of bias analysis independently, disagreement was resolved through consensus discussion. The detailed search and selection process is illustrated in Fig. 1.

Fig. 1
figure 1

The selection procedure for eligible studies was in accordance with the PRISMA guidelines

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Eligibility criteria

Comparative studies focus on mucinous and non-mucinous rectal adenocarcinoma, containing data on pathological complete response (pCR), tumor and nodal down-staging, recurrence, and survival rates. Only studies written in English are considered. Exclusion criteria include case reports, reviews, studies exclusively on mucinous cancer, or those lacking comparative data. Studies describing outcomes following surgery without neoadjuvant chemoradiotherapy (NCRT) are excluded, as well as those integrating mucinous adenocarcinoma (MAC) with signet-ring cell carcinoma. Additionally, studies where not all patients received NCRT or those on rectal cancer (RC) with mucin components after NCRT are excluded. These criteria ensure the inclusion of high-quality studies directly comparing outcomes between mucinous and non-mucinous rectal adenocarcinoma following NCRT and surgery, while excluding potential confounding factors or studies lacking relevant comparative data.

Data extraction and outcomes

The following information of eligible studies were retrieved and recorded: Authors’ names: The names of the authors of each study included in your analysis.Year of publication: The publication year of each study.Study type: Whether the study is a randomized controlled trial, cohort study, case-control study, etc.Enrollment interval: The time period during which participants were enrolled in the study.Number of LARC patients with MAC and AC: The number of patients with locally advanced rectal cancer (LARC) who had mucinous adenocarcinoma (MAC) and non-mucinous adenocarcinoma (AC), respectively.Clinical stage: The initial clinical staging of the rectal cancer patients before treatment.Regimen of NCRT: The specific protocol or regimen used for neoadjuvant chemoradiotherapy in each study.Number of males and females in each group: The gender distribution among patients with MAC and AC.pCR rate: The rate of pathological complete response among patients with MAC and AC.Tumor and nodal down-staging: The extent of down-staging of tumors and lymph nodes after neoadjuvant therapy compared to the initial clinical staging.Local recurrence rate: The rate of cancer recurrence at the site of the original tumor.Overall survival: The survival outcomes of patients with MAC and AC, typically measured from the time of diagnosis or treatment initiation.By collecting and analyzing these data points from each eligible study, you’ll be able to conduct a thorough comparative analysis of outcomes between mucinous and non-mucinous rectal adenocarcinoma following neoadjuvant chemoradiotherapy and surgery.

Risk of bias assessment

Using the Newcastle-Ottawa Scale (NOS) to assess the quality of observational studies is a common practice in systematic reviews and meta-analyses. The NOS evaluates the quality of non-randomized studies based on three domains: selection of study groups, comparability of groups, and ascertainment of either exposure or outcome. Each study can be awarded a maximum of nine points, with higher scores indicating better methodological quality.

To categorize study quality according to the standards set by the Agency for Healthcare Research and Quality (AHRQ), you can use the following criteria based on the total NOS score:

Good quality: Studies scoring 7–9 points.Fair quality: Studies scoring 4–6 points.Poor quality: Studies scoring 0–3 points.By applying these criteria to the NOS scores obtained for each observational study, you can categorize their quality as good, fair, or poor. This categorization helps ensure that only high-quality studies are given more weight in your analysis, while also considering the limitations of studies with lower quality scores.

Statistical analysis

The meta-analysis utilized R software (version 4.1.0 for macOS) to compute Odds Ratios (ORs) and 95% Confidence Intervals (CIs) based on patient counts and event occurrences in both AC and MAC groups. Pooled ORs and corresponding P values were derived using the Fleiss JL [15] method. OR < 1 favors MAC, while OR > 1 favors AC. A funnel plot assessed publication bias visually, and Thompson’s test evaluated funnel plot symmetry. Inconsistency and heterogeneity were indicated by I² and τ² statistics.

Results

Eligible studies

Fifteen studies containing comparative data on outcomes in LARC patients receiving NCRT were eligible for inclusion (Table 1). A total of 562 studies were initially enrolled, and 409 studies were removed because of duplication. 32 full-text articles were assessed for eligibility, 17 of which were excluded (Fig. 1). Finally, a total of 15 comparative studies were eligible for analysis, 6 of which were prospectively performed; the remaining 9 were retrospective. Patients from 12 studies all received NCRT, and most of the patients from the remanent 3 studies received concurrent radiotherapy and chemotherapy, and the time to surgery varied from 4 to 9 weeks (Table 1). All studies have defined MAC as mucin constituting more than 50% of the tumor volume. All studies assessed tumor (pT) down-staging by pre-NCRT clinical stage compared with post-operative pathological stage. One study defined nodal (pN) down-staging as the appearance of pathologically enlarged lymph nodes (> 3 mm) on preoperative imaging compared with postoperative non-tumor histology. The remaining 2 studies describing nodal down-staging but did not provide criteria used to assess nodal status on pre-NCRT imaging. The mean ages in the MAC group ranged from 34 to 63 years, and the mean ages in the AC group ranged from 53 to 63 years. The numbers of males and females in each group are described in Table 1. Postoperative adjuvant chemotherapy use was described in 2 of the 8 studies.

Table 1 Characteristics of included studies
Full size table

Risk of bias

The assessment of bias risk revealed that, out of the studies included, one met the criteria for a study of high quality, while 14 was deemed to be of fair quality study (Supplementary Table 1).

Pathological complete response rates

The odds ratios (ORs) of pCR for 331 MAC of LARC patients were calculated and plotted in Fig. 2. Results showed that MAC patients had a significantly poorer response rate than AC patients following NCRT (OR = 0.38; 95% CI, 0.18–0.78; p < 0.1; I2 = 46%, Fig. 2). The results of Thompson tests showed that the publication bias was significant (p < 0.05, Supplementary Fig. 1).

Fig. 2
figure 2

Meta-analysis of pathological complete response rate in mucinous and no mucinous rectal cancer patients following neoadjuvant chemoradiotherapy. Random-effects odds ratios (ORs) were calculated and plotted in the forest plot. The size of each marker varies according to the weight given to the specific study

Full size image

Tumor and nodal down-staging rates

Then, the odds ratios of tumor down-staging for 285 MAC of LARC patients were calculated and plotted in Fig. 3. Results showed that MAC patients had a significantly lower tumor down-staging rate than AC patients following NCRT (OR = 0.31; 95% CI, 0.22–0.44; p < 0.01; I2 = 21%, Fig. 3). The results of Thompson tests showed that there was no significant publication bias (p > 0.05, Supplementary Fig. 2).

Fig. 3
figure 3

Meta-analysis of tumor downstaging in mucinous and no mucinous rectal cancer patients following neoadjuvant chemoradiotherapy

Full size image

Next, the odds ratios of nodal down-staging for 199 MAC of LARC patients were calculated and plotted in Fig. 4. Surprisingly, MAC histology seemed to have no significant impact on nodal down-staging in RC patients following NCRT, but the OR value was relatively lower than AC patients (OR = 0.42; 95% CI, 0.16–1.12; p = 0.08, I2 = 88%). The results of Thompson tests showed that there was no significant publication bias (p > 0.05, Supplementary Fig. 3).

Fig. 4
figure 4

Meta-analysis of nodal downstaging in mucinous and no mucinous rectal cancer patients following neoadjuvant chemoradiotherapy

Full size image

Discussion

In this meta study, MAC of LARC was found to be an indicator of poor response to NCRT with lower rates of pCR and tumor down-staging. The nodal down-staging of MAC was relatively lower than that of AC, although the differences were not statistically significant.

MAC presents a series of ordinary features when compared with AC in terms of clinicopathological and molecular features [16,17,18,19]. Some studies have demonstrated that MAC is associated with poor tumor differentiation and advanced disease stage [20, 21]. Moreover, gene mutations such as BRAF and KRAS, abnormal expression in MUC-2, and increased frequency of microsatellite instability (MSI) have also been confirmed by a series of studies in MAC [18, 22]. However, there is no strong evidence to elucidate the potential molecular mechanisms between MAC and AC until now.

The prognostic role of MAC in colon cancer is still under debate [23,24,25]. However, MAC has been confirmed to be associated with a poor prognosis in rectal cancer [26]. Although current clinical guidelines don’t distinguish MAC from AC in management and treatment, the results of our study suggested that MAC had a poorer prognosis in terms of response rate to NCRT, as well as tumor down-staging. This might indicate that the current standard NCRT regimen is not an optimal choice for rectal MAC patients. MAC tends to have a more aggressive growth pattern, which leads to a delayed diagnosis in advanced stages [5, 27]. This characteristic could also be responsible for the lower pCR to NCRT. Another reason for the lower response to NCRT might be the oncogenic mutations in MAC, such as BRAF and KRAS mutations [22]. Owing to the large amount of mucin component present in tumor extracellular space, the induction of vessels and blood stream makes it inaccessible for chemotherapy agents delivery. Meanwhile, the mucous layer also provides a physical barrier to radiation penetration [28]. Therefore, MAC presents a poor response to NCRT according to above reasons in LARC.

Another interesting finding of this study is that although significant differences were found between MAC and AC in terms of pCR and tumor down-staging, there was no significant differences in nodal down-staging of LARC. This finding was consistent with the results of a previous meta-analysis [29]. A potential explanation is that MAC has predominantly peritoneal and distant lymphnode metastasis, and the mucous layer and mucin component may function as a barrier to the successful delivery of chemotherapy agents and radiation [28]. Another potential reason for the bias presented by this result might be the limited data on nodal down-staging.

This meta-analysis included a combination of prospective and retrospective studies from 2007 to 2021, which comprised a longer time scale than the previous meta-analysis [29]. The results of our study are generally in accordance with the former results, although 7 studies published after 2016 were added. However, a few studies have reported postoperative survival data, and the long-term prognosis of RC patients following NCRT were still unknown in these studies. Some included studies had reported that the OS of MAC was significantly worse than that of AC patients [30, 31]. Some other studies reported a poorer prognosis of MAC than AC, but the differences were not significant [11, 32]. Thus, further investigations are needed to determine the long-term prognosis of MAC following NCRT. Unavoidable limitations of this study should be acknowledged. Inaccessibility of the original data caused the heterogeneity and potential bias. Patients described in the eligibilities did not 100% receive surgery or post-operative adjuvant chemotherapy which led to the long-term survival was variable among the different studies. Finally, half of the included studies were retrospective observations, and the variations in patient populations and study designs also could cause bias.

In conclusion, although this study had some limitations, it still found that MAC of LARC was a predictor of poor response to NCRT with lower rates of pCR and tumor down-staging. The nodal down-staging of MAC was relatively lower than that of AC, although the differences were not significant. These findings will be helpful for the development and revision of LARC management guidelines in the future.

Data availability

No datasets were generated or analysed during the current study.

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Acknowledgements

This work was supported by the Natural Science Foundation of Hunan Province (2022JJ30538, 2023JJ60368) and the Scientific Research Fund Project of Hunan Provincial Health Commission (202104010105).

Funding

This work was supported by the Natural Science Foundation of Hunan Province (2022JJ30538, 2023JJ60368) and the Scientific Research Fund Project of Hunan Provincial Health Commission (20210401010).

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Authors and Affiliations

  1. The Second Affiliated Hospital, Department of Hepatobiliary Surgery, Hengyang Medical School, University of South China, Hengyang, 421001, Hunan, China

    Xiangwen Tan & Xiuda Peng

  2. The First Affiliated Hospital, Institute of Oncology, Hengyang Medical School, University of South China, Hengyang, 421001, Hunan, China

    Yiwei Zhang, Xiaofeng Wu, Qing Fang, Yunhua Xu & Shuai Xiao

  3. The First Affiliated Hospital, Department of Gastrointestinal surgery, Hengyang Medical School, University of South China, Hengyang, 421001, Hunan, China

    Shuxiang Li, Jinyi Yuan & Shuai Xiao

  4. Institute of Molecular Precision Medicine and Hunan Key Laboratory of Molecular Precision Medicine, Department of General Surgery, Xiangya Hospital, Central South University, Changsha, 410008, Hunan, China

    Kai Fu

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Contributions

Shuai Xiao, Kai Fu and Xiuda Peng contributed the study concept and study design, Xiangwen Tan, Yiwei Zhang, Xiaofeng Wu contributed to the data acquisition, quality control of data and algorithms. Xiangwen Tan and Yiwei Zhang did the data analysis and interpretation and statistical analysis. Xiaofeng WU, Shuxiang Li, Jinyi Yuan write the manuscript. Shuai Xiao, Xiuda Peng and Yunhua Xu contributed to the manuscript editing. All authors reviewed the manuscript.

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Correspondence to Xiuda Peng, Kai Fu or Shuai Xiao.

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Tan, X., Zhang, Y., Wu, X. et al. Mucinous histology is a negative predictor of neoadjuvant chemoradiotherapy for locally advanced rectal adenocarcinoma. BMC Gastroenterol 24, 263 (2024). https://doi.org/10.1186/s12876-024-03359-9

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BMC Gastroenterology

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