Retrospective Cohort Study Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Surg. Aug 27, 2024; 16(8): 2503-2510
Published online Aug 27, 2024. doi: 10.4240/wjgs.v16.i8.2503
Lymph node dissection does not affect the survival of patients with tumor node metastasis stages I and II colorectal cancer
Fan He, Shu-Pei Qu, Ye Yuan, Kun Qian, Department of Gastrointestinal Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China
ORCID number: Fan He (0009-0003-3687-1457); Kun Qian (0000-0001-8626-3976).
Co-first authors: Fan He and Shu-Pei Qu.
Author contributions: He F and Qu SP collected and analyzed the data; He F drafted the manuscript; Yuan Y completed the follow-up; Qian K designed the study; Yuan Y and Qian K reviewed the manuscript; All authors conduce to the manuscript revision and approved the submitted version.
Supported by Chongqing Medical University Future Medical Youth Innovation Team Development Support Program, No. 03030299QC-W0007.
Institutional review board statement: The study was approved by the ethics committee of the First Affiliated Hospital of Chongqing Medical University was obtained (2022-K396).
Informed consent statement: The Ethics Committee waived the requirement for informed consent.
Conflict-of-interest statement: The authors declare that they have no conflict of interest.
Data sharing statement: The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
STROBE statement: The authors have read the STROBE Statement—checklist of items, and the manuscript was prepared and revised according to the STROBE Statement—checklist of items.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Kun Qian, PhD, Chief Doctor, Department of Gastrointestinal Surgery, The First Affiliated Hospital of Chongqing Medical University, No. 1 Youyi Road, Chongqing 400016, China. hxjsqk@hotmail.com
Received: May 12, 2024
Revised: July 5, 2024
Accepted: July 9, 2024
Published online: August 27, 2024
Processing time: 96 Days and 2.6 Hours

Abstract
BACKGROUND

The effect of the number of lymph node dissections (LNDs) during radical resection for colorectal cancer (CRC) on overall survival (OS) remains controversial.

AIM

To investigate the association between the number of LNDs and OS in patients with tumor node metastasis (TNM) stage I–II CRC undergoing radical resection.

METHODS

Patients who underwent radical resection for CRC at a single-center hospital between January 2011 and December 2021 were retrospectively analyzed. Cox regression analyses were performed to identify the independent predictors of OS at different T stages.

RESULTS

A total of 2850 patients who underwent laparoscopic radical resection for CRC were enrolled. At stage T1, age [P < 0.01, hazard ratio (HR) = 1.075, 95% confidence interval (CI): 1.019-1.134] and tumour size (P = 0.021, HR = 3.635, 95%CI: 1.210-10.917) were independent risk factors for OS. At stage T2, age (P < 0.01, HR = 1.064, 95%CI: 1.032-1.098) and overall complications (P = 0.012, HR = 2.297, 95%CI: 1.200-4.397) were independent risk factors for OS. At stage T3, only age (P < 0.01, HR = 1.047, 95%CI: 1.027-1.066) was an independent risk factor for OS. At stage T4, age (P < 0.01, HR = 1.057, 95%CI: 1.039-1.075) and body mass index (P = 0. 034, HR = 0.941, 95%CI: 0.890-0.995) were independent risk factors for OS. However, there was no association between LNDs and OS in stages I and II.

CONCLUSION

The number of LDNs did not affect the survival of patients with TNM stages I and II CRC. Therefore, insufficient LNDs should not be a cause for alarm during the surgery.

Key Words: Lymph nodes; Colorectal cancer; T stage; Overall survival; Cox regression analyses

Core Tip: This retrospective cohort study aimed to investigate the association between the total number of lymph node dissections (LNDs) and overall survival (OS) in patients with tumor node metastasis stages I and II colorectal cancer who underwent laparoscopic radical resection. The results indicated that there was no association between the total number of LNDs and the OS in these patients. Therefore, insufficient LNDs should not be a cause for alarm during the surgery.
INTRODUCTION

Colorectal cancer (CRC) is the second leading cause of cancer-associated morbidity and the third leading cause of mortality worldwide[1,2]. More than 900000 people die due to CRC each year[3-5]. Radical resection is the most important form of treatment for patients with CRC; however, the rate of recurrence is approximately 40% in patients with tumor node metastasis (TNM) stage II[6-8]. The 5-year survival rate of patients with stage II CRC is 60%-80%[9]. Compared to patients in stage I, the decision to administer adjuvant chemotherapy to patients in stage II is complicated[10].

At present, the lymph node status during surgical resection is considered the strongest predictor of patient prognosis[11,12]. It is generally considered that an increase in the number of lymph nodes in CRC-resected specimens increases the possibility of identifying the involved lymph nodes[13]. Previous studies and guidelines have indicated that at least 12 Lymph nodes must be removed to ensure adequate sampling[14,15]. However, in clinical practice, the number of lymph nodes recovered varies greatly owing to many factors[16].

Some researchers have considered that extensive lymph node dissection (LND) might prolong survival, while others believe that it might increase the risk of postoperative complications without improving survival[14,17,18]. However, the effect of the number of LNDs on patient survival remains controversial.

Therefore, this study aimed to investigate the association between the total number of LNDs and overall survival (OS) in patients with TNM stages I and II CRC who underwent radical resection.

MATERIALS AND METHODS
Patients

This study included 2850 patients who underwent radical resection for CRC between January 2011 and December 2021 at the First Affiliated Hospital of Chongqing Medical University.

The inclusion criteria were as follows: (1) Pathological diagnosis of colorectal adenocarcinoma; (2) Laparoscopic radical resection for CRC; (3) Postoperative pathological stage being TNM stages I and II; and (4) Age > 18 years.

The exclusion criteria were as follows: (1) Patients who received neoadjuvant radiochemotherapy; (2) Patients with severe cardiopulmonary disease; and (3) Patients with incomplete clinical data.

Surgery management and follow-up

According to the clinical guidelines, this study enrolled all patients who underwent laparoscopic radical resection for CRC, including total mesorectal excision or complete mesocolic excision, which was pathologically confirmed as R0 resection. The patients were followed up via telephone reviews.

Definitions

The TNM stage was determined according to the American Joint Committee on Cancer 8th Edition[19]. The complications were defined according to the Clavien-Dindo classification[20]. The time interval from the date of surgery to the time of the last follow-up or death was defined as the OS.

Data collection

The baseline information included sex, age, smoking, drinking, body mass index (BMI), hypertension, type 2 diabetes mellitus, previous abdominal surgery, tumour location, T stage, tumour size, LNDs, and overall complications. All details were collected from medical records and telephone interviews.

Statistical analysis

Categorical variables are expressed as n (%), and continuous variables are expressed as the mean ± SD. Cox regression analyses were performed to identify the independent predictive factors for the OS. Data were analyzed using SPSS (version 22.0) statistical software. The level of statistical significance was set at P < 0.05.

RESULTS
Clinical characteristics

A total of 4623 patients with CRC who underwent laparoscopic radical resection for CRC and had complete medical information were included in this study. Patients with stages III or IV CRC (n = 1722) and those who received neoadjuvant radiochemotherapy (n = 51) were excluded (Figure 1). Finally, 2850 eligible patients with CRC were included in the study. The mean age was 62.8 ± 12.0 years, and 1713 (60.1%) of the patients were males. There were more cases of rectal cancers and a higher proportion of small tumours (< 5 cm). The number of patients in stages T1, T2, T3, and T4 was 270 (9.5%), 596 (20.9%), 725 (25.4%), and 1259 (44.2%), respectively. The average total number of dissected lymph nodes was 14.9 ± 7.8. Moreover, the median follow-up time was 38 (1-114) months (Table 1).

Figure 1
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Figure 1 Flow chart of patients selection. CRC: Colorectal cancer.
Table 1 Clinical characteristics of patients with colorectal cancer.
Characteristics
n (%)
Age (years)62.8 ± 12.0
Sex
Male1713 (60.1)
Female1137 (39.9)
BMI (kg/m2)22.7 ± 3.2
Smoking1110 (38.9)
Drinking898 (31.5)
Hypertension745 (26.1)
T2DM350 (12.3)
Surgical history688 (24.1)
Tumor location
Colon1363 (47.8)
Rectum1487 (52.2)
T stage
1270 (9.5)
2596 (20.9)
3725 (25.4)
41259 (44.2)
Tumor size
< 5 cm1702 (59.7)
≥ 5 cm1148 (40.3)
Total lymph nodes14.9 ± 7.8
Overall complications618 (21.7)
Follow-up (months)38 (1-114)
T2DM: Type 2 diabetes mellitus; BMI: Body mass index.
Cox regression analysis for patients with T1 stage CRC

The univariate and multivariate cox regression analyses revealed that age [hazard ratio (HR) = 1.075, 95% confidence interval (CI): 1.019-1.134, P < 0.01] and tumour size (HR = 3.635, 95%CI: 1.210-10.917, P = 0.021) were independent risk factors for the OS for patients with T1 stage CRC. However, the number of LNDs did not change the OS of these patients (HR = 0.989, 95%CI: 0.906-1.079, P = 0.807) (Table 2).

Table 2 Cox regression analysis of overall survival of T1 patients with colorectal cancer.
Risk factors
Univariate analysis
Multivariate analysis
HR (95%CI)
P value
HR (95%CI)
P value
Age (years)1.045 (1.017-1.134)0.010a1.075 (1.019-1.134)< 0.01a
Sex (male/female)0.592 (0.185-1.894)0.377
BMI (kg/m2)0.814 (0.662-1.001)0.052
T2DM (yes/no)2.696 (0.845-8.605)0.094
Tumor location (colon/rectum)2.109 (0.734-6.060)0.166
Surgical history (yes/no)0.467 (0.104-2.087)0.319
Smoking (yes/no)0.920 (0.307-2.759)0.881
Drinking (yes/no)1.046 (0.348-3.140)0.936
Hypertension (yes/no)0.852 (0.236-3.068)0.806
Tumor size (≥ 5 cm/< 5 cm)3.418 (1.134-10.299)0.029a3.635 (1.210-10.917)0.021a
Lymph nodes0.989 (0.906-1.079)0.807
Overall complications (yes/no)1.227 (0.381-3.944)0.732
aP < 0.05.
HR: Hazard ratio; CI: Confidence interval; BMI: Body mass index; T2DM: Type 2 diabetes mellitus.
Cox regression analysis for patients with T2 stage CRC

Univariate and multivariate cox regression analyses were used to identify independent predictors of the OS for patients with T2 stage CRC. Age (HR = 1.064, 95%CI: 1.032-1.098, P < 0.01) and overall complications (HR = 2.297, 95%CI: 1.200-4.397, P = 0.012) were identified as independent risk factors for the OS. However, the number of LNDs did not change the OS (HR = 0.946, 95%CI: 0.893-1.002, P = 0.057) (Table 3).

Table 3 Cox regression analysis of overall survival of T2 patients with colorectal cancer.
Risk factors
Univariate analysis
Multivariate analysis
HR (95%CI)
P value
HR (95%CI)
P value
Age (years)1.073 (1.040-1.107)< 0.01a1.064 (1.032-1.098)< 0.01a
Sex (male/female)0.718 (0.374-1.376)0.318
BMI (kg/m2)0.947 (0.856-1.047)0.290
T2DM (yes/no)2.309 (1.015-5.251)0.046a1.966 (0.862-4.485)0.108
Tumor location (colon/rectum)1.058 (0.514-2.178)0.879
Surgical history (yes/no)0.805 (0.369-1.757)0.586
Smoking (yes/no)1.008 (0.516-1.971)0.981
Drinking (yes/no)0.836 (0.383-1.825)0.653
Hypertension (yes/no)1.405 (0.708-2.791)0.331
Tumor size (≥ 5 cm/< 5 cm)0.892 (0.392-2.027)0.785
Lymph nodes0.946 (0.893-1.002)0.057
Overall complications (yes/no)2.833 (1.498-5.355)< 0.01a2.297 (1.200-4.397)0.012a
aP < 0.05.
HR: Hazard ratio; CI: Confidence interval; BMI: Body mass index; T2DM: Type 2 diabetes mellitus.
Cox regression analysis for patients with T3 stage CRC

In patients in the T3 stage, using univariate and multivariate cox regression analyses, we found that age (HR = 1.047, 95%CI: 1.027-1.066, P < 0.01) was an independent risk factor for the OS. However, the number of LNDs did not affect the OS of these patients (HR = 0.973, 95%CI: 0.946-1.002, P = 0.067) (Table 4).

Table 4 Cox regression analysis of overall survival of T3 patients with colorectal cancer.
Risk factorsUnivariate analysis
Multivariate analysis
HR (95%CI)
P value
HR (95%CI)
P value
Age (years)1.051 (1.031-1.070)< 0.01a1.047 (1.027-1.066)< 0.01a
Sex (male/female)0.840 (0.557-1.267)0.405
BMI (kg/m2)0.946 (0.890-1.006)0.079
T2DM (yes/no)2.040 (1.247-3.337)< 0.01a1.470 (0.891-2.425)0.132
Tumor location (colon/rectum)0.909 (0.612-1.351)0.638
Surgical history (yes/no)0.598 (0.340-1.021)0.059
Smoking (yes/no)1.177 (0.789-1.756)0.424
Drinking (yes/no)1.252 (0.830-1.888)0.284
Hypertension (yes/no)1.316 (0.849-2.040)0.220
Tumor size (≥ 5 cm/< 5 cm)0.969 (0.652-1.440)0.877
Lymph nodes0.973 (0.946-1.002)0.067
Overall complications (yes/no)1.777 (1.181-2.674)< 0.01a1.487 (0.983-2.250)0.060
aP < 0.05.
HR: Hazard ratio; CI: Confidence interval; BMI: Body mass index; T2DM: Type 2 diabetes mellitus.
Cox regression analysis for patients with T4 stage CRC

In these patients, we found that age (HR = 1.057, 95%CI: 1.039-1.075) and BMI (HR = 0.941, 95%CI: 0.890-0.995, P < 0.01, P = 0.034) were independent risk factors for the OS. However, the number of LNDs did not affect the OS (HR = 0.979, 95%CI: 0.955-1.003, P < 0.01) (Table 5).

Table 5 Cox regression analysis of overall survival of T4 patients with colorectal cancer.
Risk factors
Univariate analysis
Multivariate analysis
HR (95%CI)
P value
HR (95%CI)
P value
Age (years)1.061 (1.044-1.079)< 0.01a1.057 (1.039-1.075)< 0.01a
Sex (male/female)0.848 (0.589-1.219)0.373
BMI (kg/m2)0.915 (0.864-0.969)< 0.01a0.941 (0.890-0.995)0.034a
T2DM (yes/no)1.139 (0.674-1.923)0.627
Tumor location (colon/rectum)0.845 (0.599-1.192)0.337
Surgical history (yes/no)1.187 (0.803-1.756)0.390
Smoking (yes/no)1.309 (0.928-1.847)0.125
Drinking (yes/no)1.096 (0.764-1.574)0.618
Hypertension (yes/ no)1.772 (1.240-2.531)< 0.01a
Tumor size (≥ 5 cm/< 5 cm)0.875 (0.620-1.234)0.4470.855 (0.605-1.207)0.373
Lymph nodes0.979 (0.955-1.003)0.084
Overall complications (yes/no)1.766 (1.220-2.558)< 0.01a1.432 (0.982-2.088)0.062
aP < 0.05.
HR: Hazard ratio; CI: Confidence interval; BMI: Body mass index; T2DM: Type 2 diabetes mellitus.
DISCUSSION

In this study, we found that age and tumour size were independent risk factors for the OS of patients with T1-stage CRC. In the T2 stage, age and overall complications were identified as independent risk factors for the OS. In the T3 stage, age was identified as an independent risk factor for the OS. Moreover, in the T4 stage, age and BMI were independent risk factors for the OS. Nevertheless, we did not find an association between the total number of LNDs and OS in patients with TNM stages I and II CRC.

Lymph node involvement is considered the most important factor affecting the prognosis of patients with CRC after radical surgery[21-23]. Ideally, all lymph nodes in the surgical specimen should be collected and examined to accurately determine the tumour stage. However, this approach is impractical. The results of large databases such as surveillance, epidemiology, and end results showed that only approximately 40% of patients underwent sufficient lymph node examinations[24,25]. Recently, the scope of lymph node examination has become an interesting topic; however, considerable variation exists among several studies.

The number of lymph nodes required to accurately determine the tumour stage remains controversial. Current guidelines from the Joint American Cancer Commission recommend that 12 or more lymph nodes should be evaluated for accurate staging[26]. Scott et al[27] found that more than 90% of specimens with lymph node metastasis could be identified when the examination was performed on at least 13 Lymph nodes. Choi et al[28] suggested that at least 21 Lymph nodes should be examined in patients with stage II disease to accurately determine the prognosis. Sarli et al[29] found that in stage II, the survival rates of patients with negative lymph nodes were similar to those of patients with one to three positive lymph nodes, and fewer than 10 Lymph nodes were removed. In a systematic review, Chang et al[30] reported that the survival rate of patients with stages II and III colon cancer increased as the number of lymph nodes increased. However, McDonald et al[18] presented with a different opinion. They believed that an increase in the number of lymph nodes would not affect the OS. Therefore, it is necessary to explore the relationship between the total number of LNDs and OS in patients with TNM stages I and II CRC.

In the Cox regression analyses, we found many factors affecting CRC survival, including age, tumour size, and overall complications. This finding is consistent with those of previous studies[31-33]. The average total number of LNDs was 14.9 ± 7.8. Nevertheless, we did not find that the total number of LNDs affected the OS in T1-4N0M0. The mechanism is unclear, but possible reasons may be as follows: First, T1-4N0M0 is the early stage of the tumour without lymph node metastasis. Second, for early tumours, surgeons may not be as aggressive as for advanced tumours, which may cause less damage to the body.

To the best of our knowledge, this study had the largest sample size to date to reveal the relationship between LNDs and OS. However, the study had some limitations. First, this was a retrospective, single-centre study. Moreover, we excluded patients with CRC who had received neoadjuvant radiochemotherapy before surgery. Previous studies have shown that the number of recovered lymph nodes decreases after neoadjuvant therapy[34,35]. Therefore, multicentre prospective randomised controlled trials should be conducted in the future.

CONCLUSION

We found that no association between the total number of LNDs and the OS of patients with TNM stages I and II CRC. Therefore, an insufficient number of LNDs should not be a cause for alarm during surgery.

ACKNOWLEDGEMENTS

We acknowledge all the authors whose publications are referred to in our article.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Gastroenterology and hepatology

Country of origin: China

Peer-review report’s classification

Scientific Quality: Grade A

Novelty: Grade A

Creativity or Innovation: Grade B

Scientific Significance: Grade A

P-Reviewer: Rather AA S-Editor: Fan M L-Editor: A P-Editor: Zhang L

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