Retrospective Study Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Oncol. May 15, 2024; 16(5): 1869-1877
Published online May 15, 2024. doi: 10.4251/wjgo.v16.i5.1869
Clinical outcome and prognostic factors of T4N0M0 colon cancer after R0 resection: A retrospective study
Bang Liu, Zhao-Xiong Zhang, Xin-Yang Nie, Wei-Lin Sun, Yong-Jia Yan, Wei-Hua Fu, Department of General Surgery, Tianjin Medical University General Hospital, Tianjin Medical University, Tianjin 300052, China
ORCID number: Bang Liu (0000-0002-2637-0945); Yong-Jia Yan (0000-0002-9496-2766); Wei-Hua Fu (0000-0003-2576-865X).
Co-first authors: Bang Liu and Zhao-Xiong Zhang.
Co-corresponding authors: Yong-Jia Yan and Wei-Hua Fu.
Author contributions: Liu B and Zhang ZX contributed equally to this work; Liu B, Zhang ZX, Yan YJ and Fu WH designed the research study; Liu B, Zhang ZX, Nie XY and Sun WL performed the research; Liu B and Nie XY contributed analytic tools; Liu B and Zhang ZX analyzed the data and wrote the manuscript; All authors have read and approve the final manuscript.
Supported by Health Science and Technology Project of Tianjin Health Commission, No. ZC20190; Tianjin Key Medical Discipline (Specialty) Construction Project, No. TJYXZDXK-005A; and Tianjin Medical University Clinical Research Fund, No. 22ZYYLCCG04.
Institutional review board statement: The study was reviewed and approved by The Ethical Committee of Tianjin Medical University General Hospital, No. IRB2023-WZ-205.
Informed consent statement: Informed oral consent was obtained from the patients for the release of clinical data involved in this study.
Conflict-of-interest statement: The authors have no conflicts of interest to declare.
Data sharing statement: Technical appendix, statistical code, and dataset available from the corresponding author at tjmughgs_fwh@163.com. Participants gave informed oral consent for data sharing.
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: Wei-Hua Fu, MD, PhD, Professor, Surgeon, Teacher, Department of General Surgery, Tianjin Medical University General Hospital, Tianjin Medical University, No. 154 Anshan Road, Tianjin 300052, China. tjmughgs_fwh@163.com
Received: January 15, 2024
Peer-review started: January 15, 2024
First decision: February 5, 2024
Revised: February 14, 2024
Accepted: March 28, 2024
Article in press: March 28, 2024
Published online: May 15, 2024

Abstract
BACKGROUND

Paradoxically, patients with T4N0M0 (stage II, no lymph node metastasis) colon cancer have a worse prognosis than those with T2N1-2M0 (stage III). However, no previous report has addressed this issue.

AIM

To screen prognostic risk factors for T4N0M0 colon cancer and construct a prognostic nomogram model for these patients.

METHODS

Two hundred patients with T4N0M0 colon cancer were treated at Tianjin Medical University General Hospital between January 2017 and December 2021, of which 112 patients were assigned to the training cohort, and the remaining 88 patients were assigned to the validation cohort. Differences between the training and validation groups were analyzed. The training cohort was subjected to multivariate analysis to select prognostic risk factors for T4N0M0 colon cancer, followed by the construction of a nomogram model.

RESULTS

The 3-year overall survival (OS) rates were 86.2% and 74.4% for the training and validation cohorts, respectively. Enterostomy (P = 0.000), T stage (P = 0.001), right hemicolon (P = 0.025), irregular review (P = 0.040), and carbohydrate antigen 199 (CA199) (P = 0.011) were independent risk factors of OS in patients with T4N0M0 colon cancer. A nomogram model with good concordance and accuracy was constructed.

CONCLUSION

Enterostomy, T stage, right hemicolon, irregular review, and CA199 were independent risk factors for OS in patients with T4N0M0 colon cancer. The nomogram model exhibited good agreement and accuracy.

Key Words: T4N0M0 colon cancer, Prognosis, Multivariate analysis, Nomogram, Colon cancer

Core Tip: Paradoxically, patients with T4N0M0 (stage II, no lymph node metastasis) colon cancer have a worse prognosis than those with T2N1-2M0 (stage III). However, no previous report has addressed this issue. A total of 200 patients underwent radical surgery with pTNM “T4N0M0” were enrolled in this study. The clinical data and outcomes of the 200 patients were analyzed. We confirmed enterostomy, T stage, right hemicolon, irregular review, carbohydrate antigen 199 were independent risk factors of overall survival by using multivariate analysis. A nomogram model based on these factors was established to predict the prognosis of patients with T4N0M0 colon cancer.



INTRODUCTION

Colon cancer is one of the most common malignant tumors worldwide[1]. In recent decades, overall survival (OS) has improved, predominantly owing to improved surgical techniques and advances in chemoradiotherapy, accompanied by the advent of targeted therapy and checkpoint blockade immunotherapy[2]. The prognosis of colon cancer mainly depends on the cancer stage as defined by the Union for International Cancer Control and The American Joint Committee on Cancer (AJCC) TNM staging classification, which is the most widely used staging system for colon cancer. Typically, patients with a higher stage have a worse prognosis than those with a lower stage. Paradoxically, it has been observed that patients with T4N0M0 (stage II, no lymph node metastasis) colon cancer have a worse prognosis than those with T2N1-2M0 (stage III)[3-5].

Patients are tentatively staged as IIB/C according to the 8th AJCC consensus guidelines for colon cancer (primary tumor invading the serosa or surrounding adipose tissue without regional lymph node or distant metastasis)[6]. However, 28.5% of patients die within five years owing to tumor recurrence[7]. Therefore, it is important to screen for risk factors affecting the prognosis of T4N0M0 colon cancer and implement stricter treatment measures for these patients.

Herein, we aimed to explore the clinical outcomes and potential prognostic factors of OS in patients with T4N0M0 colon cancer and then utilize the identified factors to build a nomogram model for predicting OS in these patients.

MATERIALS AND METHODS
Patients

Data were collected from 227 patients with T4N0M0 colon cancer treated at Tianjin Medical University General Hospital between 2017 and 2021. Patients who met the following criteria were included: Primary colon cancer confirmed by postoperative pathology; tumor invasion of the serosa or surrounding adipose tissue without regional lymph node or distant metastasis; and complete clinicopathological data. Patients with (1) multiple primary colon cancers; (2) other types of malignant tumors; (3) perioperative death; or (4) unavailable data were excluded. A total of 200 patients were enrolled in this study (Figure 1) and were subsequently assigned to two groups: The training cohort (n = 112) and the validation cohort (n = 88). This study was approved by The Ethical Committee of Tianjin Medical University General Hospital, No. IRB2023-WZ-205.

Figure 1
Figure 1 Flowchart of the study designed. 227 patients were treated and 200 patients were enrolled into this study, which were randomly divided into training cohort and validation cohort.
Data collection

Using the inpatient system, the following patient data were collected: Sex, age, preoperative complications, preoperative carcinoembryonic antigen level, preoperative carbohydrate antigen 199 (CA199) level, tumor location, laparotomy/Laparoscopy, anastomosis/enterostomy, tumor size, pathological type, status, and whether regular review.

According to the eighth edition of AJCC TNM classification system (2017)[8], TNM staging was determined by postoperative pathological and preoperative imaging data, such as computed tomography (CT) and magnetic resonance imaging (MRI) (if necessary).

Follow-up

Follow-up included measurement of tumor markers (every 3 months), chest and abdominal CT (every 6 months) or MRI (if necessary), and endoscopy once yearly. OS was calculated as the period from the date of surgery to death from any cause.

Statistical analysis

Statistical analyses were performed using IBM SPSS Statistics for Windows, version 25.0 (IBM Corp., Armonk, NY, United States). Wilcoxon rank-sum tests, t-tests, and chi-square tests were used to detect differences between the training and validation cohorts. The nomogram model was constructed using the rms package in R Studio version 2022.07.2. The concordance and accuracy of the nomogram model were verified internally and externally. Statistical significance was set at P < 0.05.

RESULTS
Patient characteristics and survival

Table 1 summarizes the general characteristics of the 200 patients included in the study. No significant differences were observed between training and validation cohorts. The median follow-up time was 32 months (range, 6–55 months) for the training cohort and 30 (7–57) months for the validation cohort. For the training cohort, the 1- and 3-year OS rates were 96.6 and 86.2%, respectively. In the validation cohort, the 1- and 3-year OS rates were 95.1 and 74.4%, respectively.

Table 1 Clinicopathological feature of patients with T4N0M0 colon cancer.
Variables

Training cohort, n (%)
Validation cohort, n (%)
P value
All patients
118 (100)82 (100)
GenderMale47 (39.8)35 (42.7)0.687
    Female71 (60.2)47 (57.3)
Age≥ 7537 (31.4)17 (20.7)0.096
< 7581 (68.6)65 (79.3)
ObstructionYes27 (22.9)10 (12.2)0.056
    No91 (77.1)72 (87.8)
CEA (ng/mL)> 542 (35.6)41 (50.0)0.042
    ≤ 576 (64.4)41 (50.0)
CA19-9 (U/mL)> 3715 (12.7)13 (15.9)0.671
    ≤ 37103 (87.3)69 (84.1)
Surgical procedureLaparotomy27 (22.9)21 (25.6)0.657
Laparoscopy91 (77.1)61 (74.4)
Right hemicolonYes61 (51.7)37 (45.1)0.360
    No57 (48.3)45 (54.9)
EnterostomyYes15 (12.7)8 (9.8)0.519
    No103 (87.3)74 (90.2)
Tumor size (cm)≥ 6.825 (21.2)25 (30.5)0.135
    < 6.893 (78.8)57 (69.5)
Poor differentiatedYes24 (20.3)15 (18.3)0.719
    No94 (79.7)67 (81.7)
T stageT4a97 (82.2)64 (78.0)0.466
    T4b21 (17.8)18 (22.0)
Lymph node count≥ 12101 (85.6)70 (85.4)0.877
    < 1217 (14.4)12 (14.6)
Regular reviewYes76 (64.4)55 (67.1)0.696
    No42 (35.6)27 (32.9)
Independent prognostic factors of T4N0M0 colon cancer

In the univariate analysis, sex (P = 0.033), obstruction (P = 0.014), CA199 (P = 0.002), surgical procedures (P = 0.012), right hemicolon (P = 0.016), enterostomy (P = 0.000), tumor size (P = 0.004), poor differentiation (P = 0.008), T stage (P = 0.000), and irregular review (P = 0.003) were associated with a shorter OS in patients with T4N0M0 colon cancer (Table 2). However, only enterostomy [P = 0.000, hazard ratio (HR) = 13.302 (3.392–52.171)], T stage [P = 0.001, HR = 10.888 (2.809–42.199)], right hemicolon [P = 0.025, HR = 5.236 (1.229–22.308)], irregular review [P = 0.040, HR = 4.626 (1.075–19.905)], and CA199 [P = 0.011, HR = 6.315 (1.520–26.243)] were identified as independent risk factors for OS in the multivariate analysis (Table 2), as shown in the Kaplan-Meier curve in Figure 2.

Figure 2
Figure 2 Kaplan-Meier curves of overall survival for patients with T4N0M0 colon cancer in the training cohort. A: Enterostomy; B: T stage; C: Right hemicolon; D: Regular review; E: Carbohydrate antigen 199. CA199: Carbohydrate antigen 199.
Table 2 Univariate and multivariate analyses for overall survival in the training cohort.
VariablesUnivariate analysis
P value
Multivariate analysis
P value
HR (95%CI)
HR (95%CI)
GenderMale1---
Female5.755 (0.660, 50.196)0.033--
Age≥ 751.745 (0.198, 15.416)0.064--
< 751---
ObstructionYes0.785 (0.035, 17.665)0.014--
No1---
CEA (ng/mL)> 51.576 (0.497, 4.994)0.434--
≤ 51---
CA199 (U/mL)> 3720.20 (1.881, 216.893)0.0026.315 (1.520, 26.243)0.011
≤ 371-1-
Surgical procedureLaparotomy1.586 (0.130, 19.331)0.012--
Laparoscopy1---
Right hemicolonYes2.873 (0.775, 10.656)0.0165.236 (1.229, 22.308)0.025
No1-1-
EnterostomyYes6.086 (1.949, 19.007)0.00013.302 (3.392, 52.171)0.000
No1-1-
Tumor size (cm)≥ 6.82.252 (0.376, 13.489)0.004--
< 6.81---
Poor differentiatedYes4.311 (1.341, 13.856)0.008--
No1---
T stageT4a1-1-
T4b8.241 (2.500, 27.158)0.00010.888 (2.809, 42.199)0.001
Lymph node count≥ 121---
< 121.143 (0.250, 5.225)0.863--
Regular reviewYes1-1-
No5.676 (1.534, 21.000)0.0034.626 (1.075, 19.905)0.040
Nomogram model of T4N0M0 colon cancer

A nomogram model was constructed to predict the prognosis of T4N0M0 colon cancer based on the results of the multivariate Cox regression analyses (Figure 3). The probabilities of 1-, 2- and 3-year OS were predicted by calculating the points of each variable and projecting the total points to the bottom scale.

Figure 3
Figure 3 The probability of 1-, 2- and 3-yr overall survival in patients with T4N0M0 colon cancer. It can be predicted by calculating the points of each variate and projecting the total points to the bottom scale. CA199: Carbohydrate antigen 199.
Nomogram model verification

The C-index, representing the predictive ability of the nomogram model for OS, was 0.927 and 0.781 for internal and external validation of the nomogram, indicating good concordance. Both the training and validation cohorts showed good concordance between the predicted and actual 1-, 2- and 3-year OS rates in the calibration curve (Figure 4).

Figure 4
Figure 4 The calibration curves of the nomogram model in the training and validation cohorts. X-axis: The predicted overall survival (OS); y-axis: The actual OS. A-C: The 1-3 yr OS of the training cohort; D-F: The 1-3 yr OS of the validation cohort. OS: Overall survival.
DISCUSSION

The TNM staging system is widely used to predict the prognosis of colon cancer and has been extensively implemented over the past few years. In general, patients with a higher TNM stage have a worse prognosis than those with a lower stage. Paradoxically, patients with T4N0M0 (stage II, no lymph node metastasis) colon cancer were found to have a worse prognosis than those with T2N1-2M0 (stage III), as shown by data from the Surveillance, Epidemiology, and End Results (SEER) program. Similar results have been reported by the Rectal Cancer Society, Japan Colon Cancer, and other research institutes[9-11]. Therefore, it is crucial to screen for risk factors that can impact the prognosis of T4N0M0 colon cancer and implement stricter treatment measures for these patients. Herein, we found that enterostomy, T stage, right hemicolon, irregular review, and CA199 were independent risk factors for OS in patients with T4N0M0 colon cancer. Moreover, we constructed a nomogram model with good concordance and accuracy using the identified risk factors.

In a study that analyzed 109953 patients with colon cancer from the SEER dataset and End Results dataset, T4a was associated with a more favorable prognosis than T4b[12,13]. Conversely, in 2019, Baguena et al[14] reported that T4a was an independent risk factor for the prognosis of patients with colorectal cancer. Given the paradoxical results for T4a and T4b in different studies, additional factors need to be included in the AJCC TNM staging system[14].

A study from Japan[15] has reported that tumor location was strongly associated with OS in patients who underwent R0 resection for colon cancer. Using data from the National Cancer Database, Narayanan et al[16] identified patients with right- and left-sided colon cancer and revealed that poor OS was associated with right colon cancer at every stage[16]. Taieb et al[17] confirmed that right-sided tumors were more likely to be poorly differentiated, exhibiting more vascular invasion, lymphatic infiltration, microsatellite instability, and BRAF mutations[17], which may contribute to worse OS. As right and left colon cancers differ considerably in terms of clinical and biological characteristics, future clinical trials on colorectal cancer should consider the primary tumor site when determining outcomes[18].

For patients with obstructive colon cancer, enterostomy should be considered when the risk of anastomotic leakage is high, as assessed by the surgeon, or when there is a postoperative anastomotic leak requiring surgical intervention[19-21]. In our study, patients who underwent enterostomy had worse OS than those who underwent anastomosis. However, the adverse effects of enterostomy on patient prognosis have been extensively reported, with dehydration and renal impairment identified as the most common, especially in patients with ileostomy[22]. A meta-analysis has shown that patients with colon cancer who underwent diverting ileostomy and experienced dehydration had worse OS[23]. Furthermore, it has been reported that enterostomies could negatively impact the quality of life, including physical role functioning, social functioning, general health, bodily pain, and vitality[24,25]. Vasilopoulos et al[26] reported that the construction of an ileostomy could impact the patient’s nutritional status, which may deteriorate and result in reduced fluid and food intake[26]. Tripaldi[27] revealed that enterostomy was found to negatively impact sexual function in patients. These adverse outcomes may indirectly result in worse OS.

CA199 is widely used for cancer screening and follow-up in patients with gastrointestinal cancer. Herein, we found that CA199 was an independent risk factor for OS in patients with T4N0M0 colon cancer. Zhou et al[28] found that high preoperative serum CA199 levels were related to worse outcomes in patients with stage III colon cancer[28]. The optimal cutoff value of preoperative CA199 in our study was 37 U/mL, which is consistent with conventional criteria.

Our study found that irregular review was an independent risk factor for OS in patients with T4N0M0 colon cancer. Patients under irregular review had shorter OS than those under regular review, which may be related to the timely detection of risk factors, such as early recurrence of tumors, and taking intervention measures in patients under regular review.

The nomogram model can display independent risk factors that affect the outcome and visually predict survival probability[29,30]. These risk factors were selected through univariate and multivariate analyses[31,32]. Limitations are obvious. This is a single-center study, lacking data from a large multicenter sample. Therefore, more patients with T4N0M0 colon cancer need to be assessed.

CONCLUSION

Based on our findings, enterostomy, T stage, right hemicolon, irregular review, and CA199 level were identified as independent risk factors of OS. A nomogram model that combines enterostomy, T stage, right hemicolon, irregular review, and CA199 was established to predict the prognosis of patients with T4N0M0 colon cancer. Enterostomy should be performed with strict adherence to the indications.

ACKNOWLEDGEMENTS

The authors would like to thank Tianjin Medical University General Hospital for support.

Footnotes

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

Peer-review model: Single blind

Specialty type: Gastroenterology and hepatology

Country/Territory of origin: China

Peer-review report’s scientific quality classification

Grade A (Excellent): 0

Grade B (Very good): B

Grade C (Good): C

Grade D (Fair): 0

Grade E (Poor): 0

P-Reviewer: Ghannam WM, Egypt; Tangsuwanaruk T, Thailand S-Editor: Fan JR L-Editor: A P-Editor: Zhang XD

References
1.  Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71:209-249.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 50630]  [Cited by in F6Publishing: 46068]  [Article Influence: 15356.0]  [Reference Citation Analysis (47)]
2.  Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet. 2019;394:1467-1480.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1570]  [Cited by in F6Publishing: 2175]  [Article Influence: 435.0]  [Reference Citation Analysis (2)]
3.  Fang SH, Efron JE, Berho ME, Wexner SD. Dilemma of stage II colon cancer and decision making for adjuvant chemotherapy. J Am Coll Surg. 2014;219:1056-1069.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 37]  [Cited by in F6Publishing: 39]  [Article Influence: 3.9]  [Reference Citation Analysis (0)]
4.  Zhang C, Yin S, Tan Y, Huang J, Wang P, Hou W, Zhang Z, Xu H. Patient Selection for Adjuvant Chemotherapy in High-Risk Stage II Colon Cancer: A Systematic Review and Meta-Analysis. Am J Clin Oncol. 2020;43:279-287.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 14]  [Cited by in F6Publishing: 14]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
5.  Schneider NI, Langner C. Prognostic stratification of colorectal cancer patients: current perspectives. Cancer Manag Res. 2014;6:291-300.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 8]  [Cited by in F6Publishing: 22]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
6.  Rahbari NN, Bork U, Motschall E, Thorlund K, Büchler MW, Koch M, Weitz J. Molecular detection of tumor cells in regional lymph nodes is associated with disease recurrence and poor survival in node-negative colorectal cancer: a systematic review and meta-analysis. J Clin Oncol. 2012;30:60-70.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 117]  [Cited by in F6Publishing: 120]  [Article Influence: 9.2]  [Reference Citation Analysis (0)]
7.  Chen K, Collins G, Wang H, Toh JWT. Pathological Features and Prognostication in Colorectal Cancer. Curr Oncol. 2021;28:5356-5383.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 27]  [Cited by in F6Publishing: 44]  [Article Influence: 14.7]  [Reference Citation Analysis (0)]
8.  Tong GJ, Zhang GY, Liu J, Zheng ZZ, Chen Y, Niu PP, Xu XT. Comparison of the eighth version of the American Joint Committee on Cancer manual to the seventh version for colorectal cancer: A retrospective review of our data. World J Clin Oncol. 2018;9:148-161.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 46]  [Cited by in F6Publishing: 48]  [Article Influence: 8.0]  [Reference Citation Analysis (1)]
9.  Chu QD, Zhou M, Medeiros K, Peddi P. Positive surgical margins contribute to the survival paradox between patients with stage IIB/C (T4N0) and stage IIIA (T1-2N1, T1N2a) colon cancer. Surgery. 2016;160:1333-1343.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 26]  [Article Influence: 3.3]  [Reference Citation Analysis (0)]
10.  Chu QD, Zhou M, Medeiros KL, Peddi P, Kavanaugh M, Wu XC. Poor survival in stage IIB/C (T4N0) compared to stage IIIA (T1-2 N1, T1N2a) colon cancer persists even after adjusting for adequate lymph nodes retrieved and receipt of adjuvant chemotherapy. BMC Cancer. 2016;16:460.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 24]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
11.  Huang B, Mo S, Zhu L, Xu T, Cai G. The survival and clinicopathological differences between patients with stage IIIA and stage II rectal cancer: An analysis of 12,036 patients in the SEER database. Oncotarget. 2016;7:79787-79796.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 20]  [Article Influence: 3.3]  [Reference Citation Analysis (0)]
12.  Gunderson LL, Jessup JM, Sargent DJ, Greene FL, Stewart A. Revised tumor and node categorization for rectal cancer based on surveillance, epidemiology, and end results and rectal pooled analysis outcomes. J Clin Oncol. 2010;28:256-263.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 182]  [Cited by in F6Publishing: 170]  [Article Influence: 12.1]  [Reference Citation Analysis (0)]
13.  Gunderson LL, Jessup JM, Sargent DJ, Greene FL, Stewart AK. Revised TN categorization for colon cancer based on national survival outcomes data. J Clin Oncol. 2010;28:264-271.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 420]  [Cited by in F6Publishing: 392]  [Article Influence: 28.0]  [Reference Citation Analysis (0)]
14.  Baguena G, Pellino G, Frasson M, Roselló S, Cervantes A, García-Granero A, Giner F, García-Granero E. Prognostic Impact of pT Stage and Peritoneal Invasion in Locally Advanced Colon Cancer. Dis Colon Rectum. 2019;62:684-693.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 24]  [Article Influence: 4.8]  [Reference Citation Analysis (0)]
15.  Aoyama T, Kashiwabara K, Oba K, Honda M, Sadahiro S, Hamada C, Maeda H, Mayanagi S, Kanda M, Sakamoto J, Saji S, Yoshikawa T. Clinical impact of tumor location on the colon cancer survival and recurrence: analyses of pooled data from three large phase III randomized clinical trials. Cancer Med. 2017;6:2523-2530.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18]  [Cited by in F6Publishing: 20]  [Article Influence: 2.9]  [Reference Citation Analysis (0)]
16.  Narayanan S, Gabriel E, Attwood K, Boland P, Nurkin S. Association of Clinicopathologic and Molecular Markers on Stage-specific Survival of Right Versus Left Colon Cancer. Clin Colorectal Cancer. 2018;17:e671-e678.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 17]  [Article Influence: 2.8]  [Reference Citation Analysis (0)]
17.  Taieb J, Kourie HR, Emile JF, Le Malicot K, Balogoun R, Tabernero J, Mini E, Folprecht G, Van Laethem JL, Mulot C, Bouché O, Aparicio T, Michel P, Thaler J, Bridgewater J, Van Cutsem E, Perkins G, Lepage C, Salazar R, Laurent-Puig P; Pan-European Trials in Alimentary Tract Cancer (PETACC)-8 Investigators. Association of Prognostic Value of Primary Tumor Location in Stage III Colon Cancer With RAS and BRAF Mutational Status. JAMA Oncol. 2018;4:e173695.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 34]  [Cited by in F6Publishing: 44]  [Article Influence: 7.3]  [Reference Citation Analysis (0)]
18.  Lee MS, Menter DG, Kopetz S. Right Versus Left Colon Cancer Biology: Integrating the Consensus Molecular Subtypes. J Natl Compr Canc Netw. 2017;15:411-419.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 175]  [Cited by in F6Publishing: 219]  [Article Influence: 31.3]  [Reference Citation Analysis (0)]
19.  You YN, Hardiman KM, Bafford A, Poylin V, Francone TD, Davis K, Paquette IM, Steele SR, Feingold DL; On Behalf of the Clinical Practice Guidelines Committee of the American Society of Colon and Rectal Surgeons. The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Management of Rectal Cancer. Dis Colon Rectum. 2020;63:1191-1222.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 102]  [Cited by in F6Publishing: 139]  [Article Influence: 34.8]  [Reference Citation Analysis (0)]
20.  Daams F, Luyer M, Lange JF. Colorectal anastomotic leakage: aspects of prevention, detection and treatment. World J Gastroenterol. 2013;19:2293-2297.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 88]  [Cited by in F6Publishing: 78]  [Article Influence: 7.1]  [Reference Citation Analysis (0)]
21.  Rahbari NN, Weitz J, Hohenberger W, Heald RJ, Moran B, Ulrich A, Holm T, Wong WD, Tiret E, Moriya Y, Laurberg S, den Dulk M, van de Velde C, Büchler MW. Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the International Study Group of Rectal Cancer. Surgery. 2010;147:339-351.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 732]  [Cited by in F6Publishing: 787]  [Article Influence: 56.2]  [Reference Citation Analysis (4)]
22.  Shabbir J, Britton DC. Stoma complications: a literature overview. Colorectal Dis. 2010;12:958-964.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 252]  [Cited by in F6Publishing: 253]  [Article Influence: 18.1]  [Reference Citation Analysis (0)]
23.  Borucki JP, Schlaeger S, Crane J, Hernon JM, Stearns AT. Risk and consequences of dehydration following colorectal cancer resection with diverting ileostomy. A systematic review and meta-analysis. Colorectal Dis. 2021;23:1721-1732.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 12]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
24.  Näsvall P, Dahlstrand U, Löwenmark T, Rutegård J, Gunnarsson U, Strigård K. Quality of life in patients with a permanent stoma after rectal cancer surgery. Qual Life Res. 2017;26:55-64.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 83]  [Cited by in F6Publishing: 118]  [Article Influence: 14.8]  [Reference Citation Analysis (0)]
25.  Vonk-Klaassen SM, de Vocht HM, den Ouden ME, Eddes EH, Schuurmans MJ. Ostomy-related problems and their impact on quality of life of colorectal cancer ostomates: a systematic review. Qual Life Res. 2016;25:125-133.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 169]  [Cited by in F6Publishing: 205]  [Article Influence: 22.8]  [Reference Citation Analysis (0)]
26.  Vasilopoulos G, Makrigianni P, Polikandrioti M, Tsiampouris I, Karayiannis D, Margari N, Avramopoulou L, Toulia G, Fasoi G. Pre- and Post-Operative Nutrition Assessment in Patients with Colon Cancer Undergoing Ileostomy. Int J Environ Res Public Health. 2020;17.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 8]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
27.  Tripaldi C. Sexual function after stoma formation in women with colorectal cancer. Br J Nurs. 2019;28:S4-S15.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 4]  [Article Influence: 0.8]  [Reference Citation Analysis (0)]
28.  Zhou W, Yang F, Peng J, Wang F, Lin Y, Jiang W, Yang X, Li L, Lu Z, Wan D, Pan Z, Fan W. High pretreatment serum CA19-9 level predicts a poor prognosis for patients with stage III colon cancer after curative resection and adjuvant chemotherapy. J Cancer. 2019;10:3810-3818.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 17]  [Cited by in F6Publishing: 19]  [Article Influence: 3.8]  [Reference Citation Analysis (1)]
29.  Raghav K, Hwang H, Jácome AA, Bhang E, Willett A, Huey RW, Dhillon NP, Modha J, Smaglo B, Matamoros A Jr, Estrella JS, Jao J, Overman MJ, Wang X, Greco FA, Loree JM, Varadhachary GR. Development and Validation of a Novel Nomogram for Individualized Prediction of Survival in Cancer of Unknown Primary. Clin Cancer Res. 2021;27:3414-3421.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 22]  [Article Influence: 7.3]  [Reference Citation Analysis (0)]
30.  Liu S, Yu X, Yang S, Hu P, Hu Y, Chen X, Li Y, Zhang Z, Li C, Lu Q. Machine Learning-Based Radiomics Nomogram for Detecting Extramural Venous Invasion in Rectal Cancer. Front Oncol. 2021;11:610338.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 13]  [Article Influence: 4.3]  [Reference Citation Analysis (0)]
31.  Zhang J, Jin J, Ai Y, Zhu K, Xiao C, Xie C, Jin X. Computer Tomography Radiomics-Based Nomogram in the Survival Prediction for Brain Metastases From Non-Small Cell Lung Cancer Underwent Whole Brain Radiotherapy. Front Oncol. 2020;10:610691.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 9]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
32.  Zhang W, Gao P, Gao J, Wu X, Liu G, Zhang X. A Clinical Nomogram for Predicting Lymph Node Metastasis in Penile Cancer: A SEER-Based Study. Front Oncol. 2021;11:640036.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 7]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]