Not all rectal cancer patients could benefit from the surgery on the primary site

doi:10.21203/rs.3.rs-2108679/v1

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Not all rectal cancer patients could benefit from the surgery on the primary site

https://doi.org/10.21203/rs.3.rs-2108679/v1

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Purpose Pieces of evidence showed the surgery on the primary site could improve the prognosis of rectal cancer patients, but the results were inconsistent. The present study investigates whether all patients could benefit from the surgery.

Methods The rectal cancer patients diagnosed between 2010 and 2019 in the Surveillance, Epidemiology, and End Results cohort were included. Multivariable Cox regression was utilized to investigate the effect of the primary site surgery on the prognosis in total patients and stratified by the age, M stage and the number of distant metastatic organs. The propensity score matching (PSM) method was also used to balance observed covariates and Kaplan-Meier method with the log-rank test was used to exam the differences in the prognosis.

Results A total of 76,941 rectal cancer patients were included and about 68.1% received surgery. The patients with surgery have a relatively lower proportion of advanced age, higher differentiated grade, T stage, N stage, M stage, and bone, brain, lung, and liver metastasis than patients without surgery. Multivariable Cox regression showed a protective effect of the surgery on the prognosis, even in patients with advanced age, distant metastasis, and multiple organ metastasis. However, no association was found in patients with four organ metastases. The PSM also confirmed the results mentioned above.

Conclusion Not all rectal cancer patients could benefit from the surgery, especially the patients with four organ distant metastases. The results could help the clinicians to tailor targeted treatment regimens and provide a guideline for making surgical decisions.

rectal cancer

surgery on primary site

prognosis

propensity score matching

precise treatment

Colorectal cancer is the third most common malignancy and the 3rd leading cancer-related death in both males and females, with 147,950 estimated new cases and 53,200 estimated deaths in the United States in 2020[1]. Rectal cancer account for about 30% of newly diagnosed colorectal cancer patients and the 5-year survival rate was calculated to be 67%[2]. The 5-year survival may decrease to about 20% when rectal cancer progresses to distant metastasis [3–5].

Surgery is acknowledged as the cornerstone of rectal cancer treatment[6, 7]. A series of studies have suggested the improved prognosis of rectal cancer after surgery, even in patients with stage IV, including the increased overall survival rate, decreased distant recurrence rate, and prevention of complications[5, 8, 9]. However, due to the relatively lower sample size incorporated into the studies, results were not so consistent[10, 11]. Moreover, due to the heterogeneity distribution of the clinical characteristics, not all rectal cancer patients can benefit from surgical treatment in clinical practice, especially for patients with relatively advanced age and multiple organ metastases. But few studies have been published to systematically validate surgery’s effect on these patients.

National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) program, established in 1973, is an authoritative source of information on cancer incidence and survival in the United States[12]. The SEER database comprises approximately 30% of the US population, which routinely collect data on patient demographics, primary tumor site, tumor morphology and stage at diagnosis, the first course of treatment, and follow-up for vital status. It provides the basis for validating the associations between surgery and the prognosis in rectal cancer patients with relatively larger sample size and higher stability and reliability.

In this study, based on the records in the SEER datasets, we aim to investigate whether all rectal cancer patients could benefit from the surgery, especially in patients with advanced age and multiple organ metastasis. Thus, to generate an individualized accurate surgical treatment strategy for rectal cancer.

Study population

International Classification of Diseases for Oncology, 3rd edition (ICD-O-3) codes confirmed malignant rectal cancer patients in this study were retrieved from the US National Cancer Institute (NCI) open public database, SEER database. The patients diagnosed between 2010 and 2019 with definite distant metastasis information were included. The data for metastatic organs such as bone, brain, liver, and lung started in 2010, and the latest data up to date was on December 31, 2019. SEER*Stat Software version 8.4.0.1 (https://seer.cancer.gov/seerstat/) (Information Management Service, Inc. Calverton, MD, USA) was used to generate the case listing.

Ethics Statement

Cancer is a reportable disease in the United States. The data in the SEER database does not require informed patient consent. This study used previously collected deidentiﬁed data, which was deemed exempt from review by the Ethics Board of the Ethics Committee of West China Fourth Hospital and West China School of Public Health, Sichuan University.

Statistical analysis

Quantitative data were described as Mean ± standard deviation (SD). Categorical data were depicted as the number and the percentage (N, %), and the difference between groups with and without surgery was tested by chi-square or sum-rank test. Surgery on the primary site was defined as any type of rectal cancer resection, including partial colectomy, total colectomy, proctocolectomy, or proctectomy of the primary tumor. The primary outcome of our study was overall survival (OS), which was defined as the time from the diagnosis of rectal cancer to the date of all-cause death. The surgery trend and the year of diagnosis were assessed with the Cochran-Armitage trend test[13]. The multivariable Cox regression model was conducted to determine the associations between surgery and prognosis of the rectal cancer patients adjusted by age, sex, race, differentiated grade, T stage, N stage, M stage, the adjusted hazard ratios (HR) along with 95% conﬁdence intervals (CIs) for describing the likelihood of surgery associated with OS. Stratified analysis was also conducted when stratified by age (≤60 years vs. 61-80 years vs.>80 years), M stage (M0 vs. M1), and the metastatic organ numbers (1 site to 4 sites).

We used the propensity score matching (PSM) method to balance the covariables between the subjects with and without surgery according to the ratio of 1:4[14]. The propensity score distribution was plotted before and after PSM matching to verify the matching effectiveness. Overall survival was estimated using the Kaplan-Meier method, and the log-rank test compared the statistically significant differences between groups.

The IBM Statistical Package conducted statistical analyses for the Social Sciences (SPSS) version 23.0 software package for Windows (SPSS, Inc., Chicago, IL, USA). All ROC curves were conducted by MedCalc 18.2.1. Statistically significant levels were two-tailed and set at p < 0.05.

Demographic and clinical characteristics

A total of 76,941 rectal cancer patients were finally included in the present study; the flowchart of the population selection procedure is shown in Figure 1. Of these patients, 45,610 (59.3%) were males, and 31,331 (40.7%) were females; the mean age was 62.91±13.24 years. A majority of the patients were White (N=63,785, 76.1%), followed by Black (N=8,943, 10.7%), Asian or Pacific Islander (N=8,760, 10.5%), and American Indian/Alaska Native (N=823, 1.0%). About 17.5% (N=13,447) of the patients harbor distant metastasis. Of them, 1,194 (1.6%) metastasis to bone metastasis, 203 (0.3%) metastases to the brain, 9,503 (12.4%) metastases to the liver, and 4,760 (6.2%) were diagnosed with lung metastasis at diagnosis. The median survival of the patients was 81.0 months (95%CI: 79.2-82.8 months), 1-year, 3-year, and 5-year survival were 83.9%, 66.6%, and 56.2%, respectively.

The factors associated with surgery

About 68.1% of the patients underwent surgery on the primary site. Most racial groups were treated surgically, and Asian or Pacific Islander patients had a higher proportion of surgery (72.6%). In comparison, the Black harbor had the lowest surgery frequency (64.7%) (p for difference<0.001). The frequency in patients with stage IV was relatively lower than in others (27.7% vs. 77.4%; chi-square=23692.30; p <0.001). From 2010 to 2019, the frequency of the surgery significantly decreased with the year, and the decreasing trend was consistent when stratified by the M stage (chi-square=162.85; p for trend<0.001; Figure 2). The annual number of rectal cancer patients increased by about 2.5%, but the percentage of surgery decreased by about 10%.

Compared with the patients who haven’t had surgery, patients underwent surgery present to be diagnosed with relatively earlier year (Z=17.74; p<0.001) and have relatively lower proportion of advanced age (chi-square=1055.57; p<0.001), higher differentiated grade (Z=27.54; p<0.001), T stage (Z=27.44; p<0.001), N stage (Z=33.33; p<0.001), M stage (chi-square=12691.20; p<0.001) and bone (chi-square=1863.79; p<0.001), brain (chi-square=284.94; p<0.001), lung (chi-square=10147.36; p<0.001) and liver metastasis (chi-square=6530.49; p<0.001). Patients who underwent surgical resection of the primary tumor had a higher proportion of alive patients than those who did not undergo resection (chi-square=10493.53; p<0.001), While no differences were found in sex (chi-square=0.13; p=0.71) and race distribution (chi-square=0.53; p=0.60) between the patients with and without surgery. (Table 1)

The effect of the surgery on the prognosis

As shown in Table 2, the median survival of the rectal cancer patients with surgery was significantly higher than the ones without surgery (median survival: 87.44 months with surgery vs. 37.03 months without surgery; p<0.001). The multivariable Cox regression showed after adjusting for age, sex, race, differentiated grade, T stage, N stage, and M stage, surgery on the primary site was negatively associated with all-cause of death risk (HR=0.32; 95%CI: 0.31-0.33; p<0.001)

When stratified by the age of the participants, the patients all identified to have significantly higher survival than the patients without surgery in the ≤60 age group (median survival: 27.00 months with surgery; p <0.001); 61-80 age group (median survival: 114.00 months with surgery vs. 19.00 months without surgery, p<0.001) and >80 age groups (median survival: 45.00 months with surgery vs. 10.00 months without surgery, p<0.001). Multivariable Cox regression confirms the negative associations between the surgery and the death risk in all of these groups.

The results were consistent when stratified by the patients with M1 stage (median survival: 48.67 months with surgery vs. 20.13 months without surgery, p<0.001; HR=0.48; 95%CI: 0.46-0.51; p<0.001) and M0 stage (median survival:51.36 months with surgery vs. 21.90 months without surgery, p<0.001; HR=0.30; 95%CI: 0.29-0.31; p<0.001). For the patients with distant organ metastasis, surgery could significantly improve the prognosis for metastatic cancer patients with one organ metastasis (median survival: 51.36 months with surgery vs. 21.90 months without surgery, p<0.001; HR=0.45; 95%CI: 0.42-0.48; p<0.001), two organs metastases (median survival: 32.99 months with surgery vs. 16.16 months without surgery, p<0.001; HR=0.56; 95%CI: 0.49-0.65; p<0.001) and three organs metastases (median survival: 16.57 months with surgery vs. 10.30 months without surgery, p=0.004; HR=0.52; 95%CI: 0.34-0.80; p<0.001). Interestingly, for the metastatic rectal cancer patients with four organ metastases, multivariable Cox regression showed no significant associations between surgery and the mortality risk (median survival: 7.20 months with surgery vs. 8.00 months without surgery, p=0.95; HR=0.36; 95%CI: 0.02-8.36; p=0.52).

PSM suggested that the overall propensity score distribution in patients with and without surgery was comparable in all subgroups after matching (Appendix Figure 1-10). Results showed rectal cancer patients with surgery exhibited a better OS than those who did not receive surgery (chi-square=6169.67; p<0.001) (Figure 3 A). When further stratified by the age group, M stage, and the number of metastatic organs, results suggested all of the patients could benefit from the surgery (Figure 3 B-I), but not the patients with four metastatic organs (chi-square=1.08; p=0.30) (Figure 3 J).

The present study used the SEER database to investigate the effect of the surgery on the prognosis of rectal cancer. The results found that surgery on the primary could prolong the survival of rectal cancer patients, no matter in patients with advanced ages and with three or fewer organ metastasis. However, rectal cancer patients with four organ metastases could not benefit from the surgery. The results could provide a precise surgical treatment strategy for rectal cancer patients.

The study was based on a retrospective real-world study; we inevitably encounter the problem of controlling confounding factors. The present study suggested the distribution of the age, differentiated grade, T stage, N stage, M stage, and metastatic organ number showed marked differences between the patients with and without surgery, which was consistent with the previous studies[15, 16]. Many methods such as multivariable Cox regression and instrumental variable method were recommended to adjust the effect of these confounding factors. However, none of these methods alone could entirely avoid the bias[17, 18]. In this study, the multivariable Cox regression and PSM method were adopted to verify the benefit of the surgery on prognosis in different subgroups. Thus, the reliability of the results was improved.

A series of studies suggested that surgery could prolong the prognosis of rectal cancer patients. Based on 10,796 rectal cancer patients with stage I–III who underwent tumor resection, Guren and colleagues suggested the five-year survival improved from 1993–1997 to 2007–2010[19]. Zhang and colleagues conducted a pan-cancer analysis of the prognostic factors for metastatic cancer. They suggested the surgery was negatively associated with all causes of death risk for metastatic rectal cancers after adjusting for age, sex, and other clinical characteristics[20]. Consistent with these studies, our study also confirmed negative associations between surgery on the primary site and all causes of mortality, even in patients with distant metastasis and patients with advanced age (> 80 years). We also suggest the surgery could not prolong the survival in patients with four organ metastasis. Another study with 158 stage IV colorectal cancer patients indicated that resectioning the primary tumor in asymptomatic stage IV does not affect survival^{[11, 21]}. The results may be partly explained by the relatively poor prognosis and smaller sample size. Previous studies suggest that distant organ metastasis could markedly decrease the overall survival of cancer patients, and a dose-response relationship between the metastatic organs and the prognosis was observed[22, 23]. A total of 25 rectal cancer patients with four organ metastases were included in the final analysis, and the median survival was estimated to be about five months. Statistical power was not sufficient to detect a significant difference.

The present study has some limitations. First, as reported in the SEER database, the SEER database does not capture information about surgery four months after the diagnosis. Thus, the results should be explained with caution as the patients without surgery may undergo surgical treatment and therefore underestimate the effect of the surgery. Second, we did not include other treatment means, such as radiation therapy and chemotherapy, which may partly affect the associations between the surgery and prognosis. One publication comparing SEER data with SEER-Medicare data reported that the sensitivity for radiation therapy and chemotherapy acquired in the SEER database were 80% and 68%, respectively. SEER did not recommend comparing the differences in the prognosis between the patients receiving or not receiving this treatment regimens[24]. Third, the choice of receiving surgery is not only determined by the tumor characteristics of the patients but also the patients’ preferences. However, the database could not capture the patients’ intentions, which may affect the results. Fourth, the primary endpoint of this study was OS, and we did not consider the relief of the local symptoms or the quality of life. Although little evidence suggests surgery could prolong the survival in patients with four organ metastasis, they may benefit from the symptom relief. Thus, the results should be explained cautiously.

The present study suggested most rectal cancer patients received surgery after diagnosis. A series of clinical factors such as age, T stage, N stage, and M stage were associated with the surgery. The surgery on the primary site could significantly increase the prognosis of the patients, no matter in patients with different age subgroups and three or fewer organ metastasis. However, rectal cancer patients could not benefit from the surgery in patients with four organ metastases. Thus, surgical treatment should be recommended if the patient meets the indications for surgery and have willing to undergo surgery, except for the patient with four organ metastases. The results could help the clinicians to tailor target treatment regimens to the patients in the clinical practice.

Statements and Declarations

Competing Interests

We declare no competing interests.

Funding disclosures

The study was supported by the National Natural Science Foundation of China (81903398), The research start-up fund for the introduction of talents of Sichuan University (YJ2021112), Medical youth Innovation research project of Sichuan Province (Q21016).

Author contributions

JZ: conceptualization, data collection and investigation, writing original draft, critical revision. WQY: methodology, assisted in the conceptualization, formal analysis, contributed to the draft writing. JX: software, imaging analysis and the related draft revision. SYL: contributed to the methodology, writing and data curation. XW: validation, data curation, project administration. All authors read and approved the final manuscript.

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Table 1: Differences in the demographic and clinical characteristics between the rectal cancer patients with and without surgery in this study.

Factors	Patients without surgery N (%)	Patients with Surgery N (%)	Chi-square/Z	P-value
Diagnosed year			17.74	<0.001
2010	2005(25.9)	5732(74.1)
2011	2206(28.2)	5628(71.8)
2012	2184(28.0)	5625(72.0)
2013	2404(29.9)	5626(70.1)
2014	2503(30.0)	5830(70.0)
2015	2586(30.8)	5812(69.2)
2016	2687(31.4)	5858(68.6)
2017	2898(33.5)	5758(66.5)
2018	2943(33.9)	5731(66.1)
2019	3168(35.9)	5649(64.1)
Age			43.78	<0.001
≤60 years	8405(25.1)	25049(74.9)
61-80 years	10577(31.5)	23048(68.5)
>80 years	4866(53.3)	4263(46.7)
Sex			0.13	0.71
Male	14176(31.3)	31049(68.7)
Female	9672(31.2)	21311(68.8)
Race			0.53	0.60
White	18465(31.1)	40926(68.9)
Black	2619(35.3)	4799(64.7)
Asian or Pacific Islander	2100(27.4)	5575(72.6)
American Indian/Alaska Native	244(32.7)	502(67.3)
Differentiated grade			27.54	<0.001
Grade I	1779(20.1)	7059(79.9)
Grade II	11252(25.7)	32487(74.3)
Grade III	3017(40.2)	4492(59.8)
Grade IV	255(29.3)	615(70.7)
T stage			27.44	<0.001
T1	12437(41.1)	17815(58.9)
T2	1272(14.5)	7497(85.5)
T3	7127(23.7)	22989(76.3)
T4	3012(42.6)	4058(57.4)
N stage			33.33	<0.001
N0	17919(35.2)	33036(64.8)
N1	4589(24.6)	14103(75.4)
N2	1340(20.4)	5221(79.6)
M stage			12691.20	<0.001
M0	14168(22.6)	48646(77.4)
M1	9680(72.3)	3714(27.7)
Bone metastasis			1863.79	<0.001
No	20939(28.9)	51595(71.1)
Yes	1032(86.5)	161(13.5)
Brain metastasis			284.94	<0.001
No	21780(29.6)	51714(70.4)
Yes	172(83.5)	34(16.5)
Liver metastasis			10147.36	<0.001
No	15109(23.4)	49340(76.6)
Yes	7026(74.2)	2439(25.8)
Lung metastasis			6530.49	<0.001
No	18078(26.2)	50865(73.8)
Yes	3874(81.7)	867(18.3)
Metastatic organ number			113.04	<0.001
0	13735(22.0)	48813(78.0)
1	5429(68.3)	2518(31.7)
2	2688(85.7)	447(14.3)
3	387(90.2)	42(9.8)
4	23(92.0)	2(8.0)
Status			10493.53	<0.001
Alive	8664(18.1)	39265(81.9)
Dead	15184(53.7)	13095(46.3)

Table 2: The associations between surgery and prognosis of rectal cancer patients in total and stratified by different metastatic organ number subgroups

Subgroups	Survival difference		Univariable Cox regression		^aMultivariable Cox regression
Subgroups	Mean survival (Months, 95%CI)	P-value	Hazard ratio (95% CI)	P-value	Hazard ratio (95% CI)	P-value
Total population		<0.001
No surgery	37.03(36.39-37.70)		Reference	1.00	Reference	1.00
Surgery	87.44(87.01-87.88)		0.21(0.20-0.21)	<0.001	0.32(0.31-0.33)	<0.001
Age ≤60 years		<0.001
No surgery	27.00(25.88-28.12)		Reference	1.00	Reference	1.00
Surgery	-		0.18(0.17-0.18)	<0.001	0.32(0.31-0.34)	<0.001
Age 61-80 years
No surgery	19.00(18.25-19.75)		Reference	1.00	Reference	1.00
Surgery	114.00		0.23(0.22-0.24)	<0.001	0.35(0.33-0.36)	<0.001
Age >80 years		<0.001
No surgery	10.00(9.41-10.60)		Reference	1.00	Reference	1.00
Surgery	45.00(42.81-47.19)		0.33(0.32-0.35)	<0.001	0.41(0.38-0.44)	<0.001
Patients with M0 stage		<0.001
No surgery	49.08(48.14-50.01)		Reference	1.00	Reference	1.00
Surgery	90.43(89.99-90.87)		0.25(0.24-0.26)	<0.001	0.30(0.29-0.31)	<0.001
Patients with M1 stage		<0.001
No surgery	20.13(19.54-20.73)		Reference	1.00	Reference	1.00
Surgery	48.67(47.09-50.25)		0.38(0.36-0.40)	<0.001	0.48(0.46-0.51)	<0.001
Metastasis to 1 organ		<0.001
No surgery	21.90(21.07-22.73)		Reference	1.00	Reference	1.00
Surgery	51.36(49.45-53.26)		0.37(0.35-0.40)	<0.001	0.45(0.42-0.48)	<0.001
Metastasis to 2 organs		<0.001
No surgery	16.16(15.37-16.95)		Reference	1.00	Reference	1.00
Surgery	32.99(29.56-36.42)		0.49(0.44-0.56)	<0.001	0.56(0.49-0.65)	<0.001
Metastasis to 3 organs		0.004
No surgery	10.30(9.03-11.57)		Reference	1.00	Reference	1.00
Surgery	16.57(12.49-20.66)		0.62(0.44-0.88)	0.006	0.52(0.34-0.80)	<0.001
Metastasis to 4 organs		0.95
No surgery	7.20(4.11-10.29)		Reference	1.00	Reference	1.00
Surgery	8.00(0.00-19.76)		0.96(0.22-4.25)	0.95	0.36(0.02-8.36)	0.52

a: adjusted by age, sex, race, differentiated grade, T stage and N stage.

No competing interests reported.

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Not all rectal cancer patients could benefit from the surgery on the primary site

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