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Introduction

The management of locally recurrent rectal cancer (LRRC) is challenging, requiring both complex surgery and a multidisciplinary approach to optimize the chance of cure1–3. About 30–50% of instances of LRRC occur with distant metastases and, traditionally, a history of previous or current metastatic disease has often been considered a contraindication for curative treatment4,5. However, there is limited evidence on the impact of distant metastases on LRRC outcomes5–7. The improvements in outcomes for metastatic colorectal cancer8,9 are changing the paradigm of treatment for LRRC with distant metastases and question the previous approach of best supportive care in this patient group.

The aim of the present study was to assess the impact of previous or synchronous distant metastases on 3-year disease-free survival (DFS) and 3-year overall survival (OS) rates for patients with LRRC treated with curative intent.

Methods

Study population

All consecutive patients affected by LRRC who were treated at the Colorectal Surgery Unit of the National Cancer Institute of Milan (Italy) from January 2009 to September 2022 were selected from a prospectively maintained database. The database was locked in September 2023 to allow a minimum follow-up of 12 months. Authorization for the present study by the Institutional Review Board was obtained (‘SEBASTIAN’ project, protocol no. 149/2019). Based on pelvic MRI, patients with LRRC were grouped according to the classification developed at the National Cancer Institute of Milan10.

Study design and endpoints

All patients initially treated with curative intent were included in the analyses. Patients were divided into three groups: those with a previous history of distant metastatic disease, synchronous or metachronous to primary rectal cancer (M+ with primary rectal cancer); those with metastases synchronous to local relapse (LRRC with M+); and those without any previous or current history of metastases (LRRC without M+). Survival outcomes of M+ with primary rectal cancer versus LRRC with M+ versus LRRC without M+ were assessed by univariable and multivariable analyses. The primary endpoints of the study were the 3-year DFS and 3-year OS rates. Secondary endpoints were the 3-year re-local recurrence-free survival and 3-year distant progression-free survival rates for the three groups. A sub-analysis was then performed including only patients who completed the planned multimodal therapy with curative resection (or local treatment) of both LRRC and distant metastases. Details regarding the multimodal treatment for LRRC and statistical analyses are available in the Supplementary Methods.

Results

Study cohort

Of 3584 patients with primary rectal cancer, LRRC occurred in 203 patients (5.7%) in the primary institution. A further 46 patients who were treated for their primary tumour in other hospitals were treated for LRRC in the primary institution. Of the 249 patients with LRRC, 15 patients (6.0%) had M+ with primary rectal cancer, 24 patients (9.7%) had LRRC with M+, and 210 patients (84.3%) had LRRC without M+. A total of 182 patients completed the planned multimodal treatment (Fig. S1). The baseline characteristics of primary rectal cancer and LLRC are available in Tables S1, S2. Details regarding the treatment of metastatic disease are available in Table S3.

Molecular features of locally recurrent rectal cancer

KRAS was mutated in 34.8% of LRRC patients with known KRAS status, with no differences observed between groups (P = 0.561). MSI-H tumours accounted for 2.8% of LRRC patients with known microsatellite status, with no differences observed between groups (P = 0.504). All patients with LRRC with available molecular data were negative for HER2 amplification and BRAF mutation. Next-generation sequencing (NGS) results from surgical specimens or biopsies were available for 14 LRRC patients. The genes that were most frequently mutated were TP53 (85.7%), APC (57.1%), and KRAS (50.0%), as can be seen in the complete NGS panel (Fig. S2).

Survival analyses for all included patients and specifically for patients who completed the planned multimodal treatment

The median follow-up was 32.6 (range 6–152) months. LRRC without M+ patients had a 3-year DFS rate of 43.8%, whereas M+ with primary rectal cancer patients had a 3-year DFS rate of 34.3%. LRRC with M+ patients had a 3-year DFS rate of 11.1% (log rank P = 0.003) (Fig. 1a). The 3-year OS rates were 77.5%, 57.3%, and 56.0% respectively (log rank P = 0.064) (Fig. 1b). When the same outcomes were analysed considering only the 182 patients who completed the planned multimodal treatment, no differences were observed between groups. Indeed, the 3-year DFS rates were 56.3% for M+ with primary rectal cancer patients, 11.4% for LRRC with M+ patients, and 50.6% for LRRC without M+ patients (log rank P = 0.098, P for trend = 0.034) (Fig. 1c). The 3-year OS rates were 71.1%, 54.5%, and 81.5% respectively (log rank P = 0.077) (Fig. 1d). Analyses of secondary endpoints are available in the Supplementary Results (Fig. S3).

Survival
Fig. 1

Survival

Open in new tabDownload slide
a Disease-free survival for patients with previous metastases and primary rectal cancer, for patients with locally recurrent rectal cancer with concurrent distant metastases, and for patients with locally recurrent rectal cancer without concurrent distant metastases. b Overall survival for patients with previous metastases and primary rectal cancer, for patients with locally recurrent rectal cancer with concurrent distant metastases, and for patients with locally recurrent rectal cancer without concurrent distant metastases. c Disease-free survival specifically for patients who completed the planned multimodal treatment with curative intent. d Overall survival specifically for patients who completed the planned multimodal treatment with curative intent. LRRC, locally recurrent rectal cancer.

Predictors of worse disease-free survival for LRRC patients

The only independent predictors of worse DFS that emerged from multivariable Cox analyses were R+ surgery for LRRC (HR 3.07, 95% c.i. 1.87 to 5.10; P < 0.001) and distant metastases synchronous to LRRC (HR 1.72, 95% c.i. 0.99 to 2.86; P = 0.044). LRRC resection with curative intent was independently associated with improved DFS, especially in the case of extended colorectal re-excision (HR 0.38, 95%c.i. 0.19–0.71, P = 0.003). The results of the Cox analyses are available in Table 1.

Table 1
Open in new tab

Univariable and multivariable Cox regression analyses for disease-free survival

UnivariableMultivariable
HR (95% c.i.)PHR (95% c.i.)P
Distance from the anal verge1.00 (0.96, 1.03)0.958––
Multimodal therapy for primary tumour
 Chemoradiation2.11 (1.35, 3.41)0.0021.06 (0.52, 2.13)0.880
 Chemo only2.23 (1.31, 3.82)0.0031.74 (0.77, 3.95)0.186
 NoneReferenceReferenceReferenceReference
(y)pT stage of primary tumour
 ypT0–2ReferenceReferenceReferenceReference
 ypT31.82 (1.19, 2.86)0.0071.31 (0.69, 2.57)0.426
 ypT42.15 (1.21, 3.76)0.0081.35 (0.61, 2.96)0.46
(y)pN stage of primary tumour
 ypN0ReferenceReferenceReferenceReference
 ypN11.95 (1.17, 3.16)0.0081.15 (0.71, 1.90)0.569
 ypN21.94 (1.30, 2.88)0.0011.66 (0.91, 2.97)0.091
Localization of LRRC
 S1a–bReferenceReferenceReferenceReference
 S1c1.29 (0.79, 2.11)0.3110.73 (0.39, 1.32)0.298
 S21.38 (0.77, 2.41)0.2620.55 (0.26, 1.13)0.109
 S31.77 (1.12, 2.83)0.0160.71 (0.41, 1.25)0.238
Multivisceral involvement
 Yes1.10 (0.69, 1.68)0.671––
 NoReferenceReference––
Lateral pelvic sidewall involvement
 Yes1.38 (0.94, 2.00)0.091––
 NoReferenceReference––
Margin status of LRRC
 R0ReferenceReferenceReferenceReference
 R+3.65 (2.52, 5.36)<0.0013.07 (1.87, 5.10)<0.001
Type of surgery
 Rectal re-excision0.32 (0.21, 0.48)<0.0010.50 (0.29, 0.85)0.012
 Extended rectal re-excision0.33 (0.19, 0.57)<0.0010.38 (0.19, 0.71)0.003
 Partial/total exenteration0.45 (0.20, 0.90)0.0370.49 (0.19, 1.13)0.109
 Re-excision with sacrectomy0.26 (0.09, 0.61)0.0051.13 (0.34, 3.30)0.831
 No resection/othersReferenceReferenceReferenceReference
Timing of metastatic occurrence
 Synchronous or metachronous to primary1.92 (0.94, 3.50)0.0511.29 (0.57, 2.61)0.512
 Synchronous to LRRC2.21 (1.34, 3.48)0.0011.72 (0.99, 2.86)0.044
 No metastasesReferenceReferenceReferenceReference
Metastasis dominant location
 Liver1.25 (0.49, 3.37)0.645––
 Lung0.82 (0.33, 2.13)0.67––
 OthersReferenceReference––
Peritoneal metastases
 Yes1.11 (0.48, 2.35)0.801––
 NoReferenceReference––
UnivariableMultivariable
HR (95% c.i.)PHR (95% c.i.)P
Distance from the anal verge1.00 (0.96, 1.03)0.958––
Multimodal therapy for primary tumour
 Chemoradiation2.11 (1.35, 3.41)0.0021.06 (0.52, 2.13)0.880
 Chemo only2.23 (1.31, 3.82)0.0031.74 (0.77, 3.95)0.186
 NoneReferenceReferenceReferenceReference
(y)pT stage of primary tumour
 ypT0–2ReferenceReferenceReferenceReference
 ypT31.82 (1.19, 2.86)0.0071.31 (0.69, 2.57)0.426
 ypT42.15 (1.21, 3.76)0.0081.35 (0.61, 2.96)0.46
(y)pN stage of primary tumour
 ypN0ReferenceReferenceReferenceReference
 ypN11.95 (1.17, 3.16)0.0081.15 (0.71, 1.90)0.569
 ypN21.94 (1.30, 2.88)0.0011.66 (0.91, 2.97)0.091
Localization of LRRC
 S1a–bReferenceReferenceReferenceReference
 S1c1.29 (0.79, 2.11)0.3110.73 (0.39, 1.32)0.298
 S21.38 (0.77, 2.41)0.2620.55 (0.26, 1.13)0.109
 S31.77 (1.12, 2.83)0.0160.71 (0.41, 1.25)0.238
Multivisceral involvement
 Yes1.10 (0.69, 1.68)0.671––
 NoReferenceReference––
Lateral pelvic sidewall involvement
 Yes1.38 (0.94, 2.00)0.091––
 NoReferenceReference––
Margin status of LRRC
 R0ReferenceReferenceReferenceReference
 R+3.65 (2.52, 5.36)<0.0013.07 (1.87, 5.10)<0.001
Type of surgery
 Rectal re-excision0.32 (0.21, 0.48)<0.0010.50 (0.29, 0.85)0.012
 Extended rectal re-excision0.33 (0.19, 0.57)<0.0010.38 (0.19, 0.71)0.003
 Partial/total exenteration0.45 (0.20, 0.90)0.0370.49 (0.19, 1.13)0.109
 Re-excision with sacrectomy0.26 (0.09, 0.61)0.0051.13 (0.34, 3.30)0.831
 No resection/othersReferenceReferenceReferenceReference
Timing of metastatic occurrence
 Synchronous or metachronous to primary1.92 (0.94, 3.50)0.0511.29 (0.57, 2.61)0.512
 Synchronous to LRRC2.21 (1.34, 3.48)0.0011.72 (0.99, 2.86)0.044
 No metastasesReferenceReferenceReferenceReference
Metastasis dominant location
 Liver1.25 (0.49, 3.37)0.645––
 Lung0.82 (0.33, 2.13)0.67––
 OthersReferenceReference––
Peritoneal metastases
 Yes1.11 (0.48, 2.35)0.801––
 NoReferenceReference––

LRRC, locally recurrent rectal cancer.

Table 1
Open in new tab

Univariable and multivariable Cox regression analyses for disease-free survival

UnivariableMultivariable
HR (95% c.i.)PHR (95% c.i.)P
Distance from the anal verge1.00 (0.96, 1.03)0.958––
Multimodal therapy for primary tumour
 Chemoradiation2.11 (1.35, 3.41)0.0021.06 (0.52, 2.13)0.880
 Chemo only2.23 (1.31, 3.82)0.0031.74 (0.77, 3.95)0.186
 NoneReferenceReferenceReferenceReference
(y)pT stage of primary tumour
 ypT0–2ReferenceReferenceReferenceReference
 ypT31.82 (1.19, 2.86)0.0071.31 (0.69, 2.57)0.426
 ypT42.15 (1.21, 3.76)0.0081.35 (0.61, 2.96)0.46
(y)pN stage of primary tumour
 ypN0ReferenceReferenceReferenceReference
 ypN11.95 (1.17, 3.16)0.0081.15 (0.71, 1.90)0.569
 ypN21.94 (1.30, 2.88)0.0011.66 (0.91, 2.97)0.091
Localization of LRRC
 S1a–bReferenceReferenceReferenceReference
 S1c1.29 (0.79, 2.11)0.3110.73 (0.39, 1.32)0.298
 S21.38 (0.77, 2.41)0.2620.55 (0.26, 1.13)0.109
 S31.77 (1.12, 2.83)0.0160.71 (0.41, 1.25)0.238
Multivisceral involvement
 Yes1.10 (0.69, 1.68)0.671––
 NoReferenceReference––
Lateral pelvic sidewall involvement
 Yes1.38 (0.94, 2.00)0.091––
 NoReferenceReference––
Margin status of LRRC
 R0ReferenceReferenceReferenceReference
 R+3.65 (2.52, 5.36)<0.0013.07 (1.87, 5.10)<0.001
Type of surgery
 Rectal re-excision0.32 (0.21, 0.48)<0.0010.50 (0.29, 0.85)0.012
 Extended rectal re-excision0.33 (0.19, 0.57)<0.0010.38 (0.19, 0.71)0.003
 Partial/total exenteration0.45 (0.20, 0.90)0.0370.49 (0.19, 1.13)0.109
 Re-excision with sacrectomy0.26 (0.09, 0.61)0.0051.13 (0.34, 3.30)0.831
 No resection/othersReferenceReferenceReferenceReference
Timing of metastatic occurrence
 Synchronous or metachronous to primary1.92 (0.94, 3.50)0.0511.29 (0.57, 2.61)0.512
 Synchronous to LRRC2.21 (1.34, 3.48)0.0011.72 (0.99, 2.86)0.044
 No metastasesReferenceReferenceReferenceReference
Metastasis dominant location
 Liver1.25 (0.49, 3.37)0.645––
 Lung0.82 (0.33, 2.13)0.67––
 OthersReferenceReference––
Peritoneal metastases
 Yes1.11 (0.48, 2.35)0.801––
 NoReferenceReference––
UnivariableMultivariable
HR (95% c.i.)PHR (95% c.i.)P
Distance from the anal verge1.00 (0.96, 1.03)0.958––
Multimodal therapy for primary tumour
 Chemoradiation2.11 (1.35, 3.41)0.0021.06 (0.52, 2.13)0.880
 Chemo only2.23 (1.31, 3.82)0.0031.74 (0.77, 3.95)0.186
 NoneReferenceReferenceReferenceReference
(y)pT stage of primary tumour
 ypT0–2ReferenceReferenceReferenceReference
 ypT31.82 (1.19, 2.86)0.0071.31 (0.69, 2.57)0.426
 ypT42.15 (1.21, 3.76)0.0081.35 (0.61, 2.96)0.46
(y)pN stage of primary tumour
 ypN0ReferenceReferenceReferenceReference
 ypN11.95 (1.17, 3.16)0.0081.15 (0.71, 1.90)0.569
 ypN21.94 (1.30, 2.88)0.0011.66 (0.91, 2.97)0.091
Localization of LRRC
 S1a–bReferenceReferenceReferenceReference
 S1c1.29 (0.79, 2.11)0.3110.73 (0.39, 1.32)0.298
 S21.38 (0.77, 2.41)0.2620.55 (0.26, 1.13)0.109
 S31.77 (1.12, 2.83)0.0160.71 (0.41, 1.25)0.238
Multivisceral involvement
 Yes1.10 (0.69, 1.68)0.671––
 NoReferenceReference––
Lateral pelvic sidewall involvement
 Yes1.38 (0.94, 2.00)0.091––
 NoReferenceReference––
Margin status of LRRC
 R0ReferenceReferenceReferenceReference
 R+3.65 (2.52, 5.36)<0.0013.07 (1.87, 5.10)<0.001
Type of surgery
 Rectal re-excision0.32 (0.21, 0.48)<0.0010.50 (0.29, 0.85)0.012
 Extended rectal re-excision0.33 (0.19, 0.57)<0.0010.38 (0.19, 0.71)0.003
 Partial/total exenteration0.45 (0.20, 0.90)0.0370.49 (0.19, 1.13)0.109
 Re-excision with sacrectomy0.26 (0.09, 0.61)0.0051.13 (0.34, 3.30)0.831
 No resection/othersReferenceReferenceReferenceReference
Timing of metastatic occurrence
 Synchronous or metachronous to primary1.92 (0.94, 3.50)0.0511.29 (0.57, 2.61)0.512
 Synchronous to LRRC2.21 (1.34, 3.48)0.0011.72 (0.99, 2.86)0.044
 No metastasesReferenceReferenceReferenceReference
Metastasis dominant location
 Liver1.25 (0.49, 3.37)0.645––
 Lung0.82 (0.33, 2.13)0.67––
 OthersReferenceReference––
Peritoneal metastases
 Yes1.11 (0.48, 2.35)0.801––
 NoReferenceReference––

LRRC, locally recurrent rectal cancer.

Discussion

Two recent studies demonstrated that 5.6–6.4% of rectal cancer patients experience local recurrence during their follow-up and up to 41–44.9% of these patients have metastases11,12. Excluding patients with known distant metastases, approximately 30% of patients with LRRC have indeterminate lung nodules observed at diagnosis13. Despite this clinical issue, there is limited evidence about the outcomes of LRRC patients with distant metastases5,7.

The present study demonstrates that patients with LRRC with a previous history of distant metastases can be considered for treatment with curative intent. The timing of the identification of distant metastases impacts on survival, as M+ with primary rectal cancer patients had improved survival compared with LRRC with M+ patients, with 3-year DFS rates of 34.3% and 11.1% respectively (log rank P = 0.003). Interestingly, when outcomes were analysed only for patients who completed the planned multimodal treatment with curative intent, a difference in the 3-year DFS rate was no longer observed between groups (log rank P = 0.098). These findings suggest that even distant metastases concurrent to LRRC could have a negligible impact on survival, when all metastatic sites are treated with a multimodal approach. Patients who had LRRC with M+ had a higher rate of R+ pelvic surgery and a higher frequency of lateral localization. Treatment with curative intent in this cohort is more challenging14,15. A recent paper from the PelvEx Collaborative demonstrated that combined surgery is feasible, with a 30-day mortality rate of 1.6% and major post-operative complications in 32% of patients; however, only primary rectal cancer was included16.

The present study has some limitations, including its retrospective nature and the relatively small sample size. Furthermore, only 15.7% of included LRRC patients had a current or previous history of distant metastases, suggesting a selection bias since only patients in whom multimodal treatment was established with curative intent were included.

In conclusion, a previous history of metastatic disease does not represent an absolute contraindication to multimodal treatment with curative intent in LRRC patients. Conversely, patients with distant lesions occurring synchronous to LRRC should be carefully selected for any attempt of curative treatment.

Funding

The authors have no funding to declare.

Acknowledgements

L.S. and E.D. contributed equally to the present work.

Disclosure

The authors declare no conflict of interest.

Supplementary material

Supplementary material is available at BJS Open online.

Data availability

Data will be available upon request to the corresponding author.

Author contributions

Luca Sorrentino (Conceptualization, Data curation, Methodology, Writing—original draft), Elena Daveri (Formal analysis), Filiberto Belli (Supervision, Writing—review & editing), Raffaella Vigorito (Data curation, Formal analysis), Luigi Battaglia (Investigation, Writing—original draft), Giovanna Sabella (Data curation, Writing—original draft), Filippo Patti (Data curation, Formal analysis), Giovanni Randon (Data curation), Filippo Pietrantonio (Supervision), Claudio Vernieri (Data curation), Davide Scaramuzza (Data curation), Sergio Villa (Data curation, Writing—review & editing), Massimo Milione (Data curation, Supervision, Writing—review & editing), Alessandro Gronchi (Supervision), Maurizio Cosimelli (Supervision), and Marcello Guaglio (Conceptualization, Investigation, Writing—review & editing)

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© The Author(s) 2024. Published by Oxford University Press on behalf of BJS Foundation Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Topic:
Subject
Lower Gastrointestinal Surgery
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Short report
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