Skip to main content
Top
Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Colon Cancer | Research

Novel nomograms to predict lymph node metastasis and liver metastasis in patients with early colon carcinoma

Authors: Yongcong Yan, Haohan Liu, Kai Mao, Mengyu Zhang, Qianlei Zhou, Wei Yu, Bingchao Shi, Jie Wang, Zhiyu Xiao

Published in: Journal of Translational Medicine | Issue 1/2019

Login to get access

Abstract

Background

Lymph node status and liver metastasis (LIM) are important in determining the prognosis of early colon carcinoma. We attempted to develop and validate nomograms to predict lymph node metastasis (LNM) and LIM in patients with early colon carcinoma.

Methods

A total of 32,819 patients who underwent surgery for pT1 or pT2 colon carcinoma were enrolled in the study based on their records in the SEER database. Risk factors for LNM and LIM were assessed based on univariate and multivariate binary logistic regression. The C-index and calibration plots were used to evaluate LNM and LIM model discrimination. The predictive accuracy and clinical values of the nomograms were measured by decision curve analysis. The predictive nomograms were further validated in the internal testing set.

Results

The LNM nomogram, consisting of seven features, achieved the same favorable prediction efficacy as the five-feature LIM nomogram. The calibration curves showed perfect agreement between nomogram predictions and actual observations. The decision curves indicated the clinical usefulness of the prediction nomograms. Receiver operating characteristic curves indicated good discrimination in the training set (area under the curve [AUC] = 0.667, 95% CI 0.661–0.673) and the testing set (AUC = 0.658, 95% CI 0.649–0.667) for the LNM nomogram and encouraging performance in the training set (AUC = 0.766, 95% CI 0.760–0.771) and the testing set (AUC = 0.825, 95% CI 0.818–0.832) for the LIM nomogram.

Conclusion

Novel validated nomograms for patients with early colon carcinoma can effectively predict the individualized risk of LNM and LIM, and this predictive power may help doctors formulate suitable individual treatments.
Literature
1.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68:7–30.CrossRef Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68:7–30.CrossRef
2.
go back to reference Benson AB 3rd, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, Cohen S, Cooper HS, Deming D, Engstrom PF, et al. NCCN Guidelines insights: colon cancer, Version 2. 2018. J Natl Compr Canc Netw. 2018;16:359–69.CrossRef Benson AB 3rd, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, Cohen S, Cooper HS, Deming D, Engstrom PF, et al. NCCN Guidelines insights: colon cancer, Version 2. 2018. J Natl Compr Canc Netw. 2018;16:359–69.CrossRef
3.
go back to reference Ulintz PJ, Greenson JK, Wu R, Fearon ER, Hardiman KM. Lymph node metastases in colon cancer are polyclonal. Clin Cancer Res. 2018;24:2214–24.CrossRef Ulintz PJ, Greenson JK, Wu R, Fearon ER, Hardiman KM. Lymph node metastases in colon cancer are polyclonal. Clin Cancer Res. 2018;24:2214–24.CrossRef
4.
go back to reference Edge SB, American Joint Committee on Cancer, American Cancer Society. AJCC cancer staging handbook : from the AJCC cancer staging manual. 7th ed. New York: Springer; 2010. Edge SB, American Joint Committee on Cancer, American Cancer Society. AJCC cancer staging handbook : from the AJCC cancer staging manual. 7th ed. New York: Springer; 2010.
5.
go back to reference Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006;244:254–9.CrossRef Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006;244:254–9.CrossRef
6.
go back to reference Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, Jemal A. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67:177–93.CrossRef Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, Jemal A. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67:177–93.CrossRef
7.
go back to reference Berger AC, Sigurdson ER, LeVoyer T, Hanlon A, Mayer RJ, Macdonald JS, Catalano PJ, Haller DG. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol. 2005;23:8706–12.CrossRef Berger AC, Sigurdson ER, LeVoyer T, Hanlon A, Mayer RJ, Macdonald JS, Catalano PJ, Haller DG. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol. 2005;23:8706–12.CrossRef
8.
go back to reference Yamaoka Y, Kinugasa Y, Shiomi A, Yamaguchi T, Kagawa H, Yamakawa Y, Furutani A, Manabe S. The distribution of lymph node metastases and their size in colon cancer. Langenbecks Arch Surg. 2017;402:1213–21.CrossRef Yamaoka Y, Kinugasa Y, Shiomi A, Yamaguchi T, Kagawa H, Yamakawa Y, Furutani A, Manabe S. The distribution of lymph node metastases and their size in colon cancer. Langenbecks Arch Surg. 2017;402:1213–21.CrossRef
9.
go back to reference Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst. 2007;99:433–41.CrossRef Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst. 2007;99:433–41.CrossRef
10.
go back to reference Isella C, Mellano A, Galimi F, Petti C, Capussotti L, De Simone M, Bertotti A, Medico E, Muratore A. MACC1 mRNA levels predict cancer recurrence after resection of colorectal cancer liver metastases. Ann Surg. 2013;257:1089–95.CrossRef Isella C, Mellano A, Galimi F, Petti C, Capussotti L, De Simone M, Bertotti A, Medico E, Muratore A. MACC1 mRNA levels predict cancer recurrence after resection of colorectal cancer liver metastases. Ann Surg. 2013;257:1089–95.CrossRef
11.
go back to reference Sargent DJ, Shi Q, Gill S, Louvet C, Everson RB, Kellner U, Clancy TE, Pipas JM, Resnick MB, Meyers MO, et al. Molecular testing for lymph node metastases as a determinant of colon cancer recurrence: results from a retrospective multicenter study. Clin Cancer Res. 2014;20:4361–9.CrossRef Sargent DJ, Shi Q, Gill S, Louvet C, Everson RB, Kellner U, Clancy TE, Pipas JM, Resnick MB, Meyers MO, et al. Molecular testing for lymph node metastases as a determinant of colon cancer recurrence: results from a retrospective multicenter study. Clin Cancer Res. 2014;20:4361–9.CrossRef
12.
go back to reference Kluth LA, Black PC, Bochner BH, Catto J, Lerner SP, Stenzl A, Sylvester R, Vickers AJ, Xylinas E, Shariat SF. Prognostic and prediction tools in bladder cancer: a comprehensive review of the literature. Eur Urol. 2015;68:238–53.CrossRef Kluth LA, Black PC, Bochner BH, Catto J, Lerner SP, Stenzl A, Sylvester R, Vickers AJ, Xylinas E, Shariat SF. Prognostic and prediction tools in bladder cancer: a comprehensive review of the literature. Eur Urol. 2015;68:238–53.CrossRef
13.
go back to reference Balachandran VP, Gonen M, Smith JJ, DeMatteo RP. Nomograms in oncology: more than meets the eye. Lancet Oncol. 2015;16:e173–80.CrossRef Balachandran VP, Gonen M, Smith JJ, DeMatteo RP. Nomograms in oncology: more than meets the eye. Lancet Oncol. 2015;16:e173–80.CrossRef
14.
go back to reference Fakhry C, Zhang Q, Nguyen-Tan PF, Rosenthal DI, Weber RS, Lambert L, Trotti AM 3rd, Barrett WL, Thorstad WL, Jones CU, et al. Development and validation of nomograms predictive of overall and progression-free survival in patients with oropharyngeal cancer. J Clin Oncol. 2017;35:4057–65.CrossRef Fakhry C, Zhang Q, Nguyen-Tan PF, Rosenthal DI, Weber RS, Lambert L, Trotti AM 3rd, Barrett WL, Thorstad WL, Jones CU, et al. Development and validation of nomograms predictive of overall and progression-free survival in patients with oropharyngeal cancer. J Clin Oncol. 2017;35:4057–65.CrossRef
15.
go back to reference Lee CK, Goldstein D, Gibbs E, Joensuu H, Zalcberg J, Verweij J, Casali PG, Maki RG, Cioffi A, McArthur G, et al. Development and validation of prognostic nomograms for metastatic gastrointestinal stromal tumour treated with imatinib. Eur J Cancer. 2015;51:852–60.CrossRef Lee CK, Goldstein D, Gibbs E, Joensuu H, Zalcberg J, Verweij J, Casali PG, Maki RG, Cioffi A, McArthur G, et al. Development and validation of prognostic nomograms for metastatic gastrointestinal stromal tumour treated with imatinib. Eur J Cancer. 2015;51:852–60.CrossRef
16.
go back to reference Ganly I, Amit M, Kou L, Palmer FL, Migliacci J, Katabi N, Yu C, Kattan MW, Binenbaum Y, Sharma K, et al. Nomograms for predicting survival and recurrence in patients with adenoid cystic carcinoma. An international collaborative study. Eur J Cancer. 2015;51:2768–76.CrossRef Ganly I, Amit M, Kou L, Palmer FL, Migliacci J, Katabi N, Yu C, Kattan MW, Binenbaum Y, Sharma K, et al. Nomograms for predicting survival and recurrence in patients with adenoid cystic carcinoma. An international collaborative study. Eur J Cancer. 2015;51:2768–76.CrossRef
17.
go back to reference Mitra AP, Lam LL, Ghadessi M, Erho N, Vergara IA, Alshalalfa M, Buerki C, Haddad Z, Sierocinski T, Triche TJ, et al. Discovery and validation of novel expression signature for postcystectomy recurrence in high-risk bladder cancer. J Natl Cancer Inst. 2014;106:290.CrossRef Mitra AP, Lam LL, Ghadessi M, Erho N, Vergara IA, Alshalalfa M, Buerki C, Haddad Z, Sierocinski T, Triche TJ, et al. Discovery and validation of novel expression signature for postcystectomy recurrence in high-risk bladder cancer. J Natl Cancer Inst. 2014;106:290.CrossRef
18.
go back to reference Gravis G, Boher JM, Fizazi K, Joly F, Priou F, Marino P, Latorzeff I, Delva R, Krakowski I, Laguerre B, et al. Prognostic factors for survival in noncastrate metastatic prostate cancer: validation of the glass model and development of a novel simplified prognostic model. Eur Urol. 2015;68:196–204.CrossRef Gravis G, Boher JM, Fizazi K, Joly F, Priou F, Marino P, Latorzeff I, Delva R, Krakowski I, Laguerre B, et al. Prognostic factors for survival in noncastrate metastatic prostate cancer: validation of the glass model and development of a novel simplified prognostic model. Eur Urol. 2015;68:196–204.CrossRef
19.
go back to reference Sauerbrei W, Boulesteix AL, Binder H. Stability investigations of multivariable regression models derived from low- and high-dimensional data. J Biopharm Stat. 2011;21:1206–31.CrossRef Sauerbrei W, Boulesteix AL, Binder H. Stability investigations of multivariable regression models derived from low- and high-dimensional data. J Biopharm Stat. 2011;21:1206–31.CrossRef
20.
go back to reference Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMJ. 2015;350:g7594.CrossRef Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMJ. 2015;350:g7594.CrossRef
21.
go back to reference Kramer AA, Zimmerman JE. Assessing the calibration of mortality benchmarks in critical care: the Hosmer–Lemeshow test revisited. Crit Care Med. 2007;35:2052–6.CrossRef Kramer AA, Zimmerman JE. Assessing the calibration of mortality benchmarks in critical care: the Hosmer–Lemeshow test revisited. Crit Care Med. 2007;35:2052–6.CrossRef
22.
go back to reference Vickers AJ, Cronin AM, Elkin EB, Gonen M. Extensions to decision curve analysis, a novel method for evaluating diagnostic tests, prediction models and molecular markers. BMC Med Inform Decis Mak. 2008;8:53.CrossRef Vickers AJ, Cronin AM, Elkin EB, Gonen M. Extensions to decision curve analysis, a novel method for evaluating diagnostic tests, prediction models and molecular markers. BMC Med Inform Decis Mak. 2008;8:53.CrossRef
23.
go back to reference Vickers AJ, Elkin EB. Decision curve analysis: a novel method for evaluating prediction models. Med Decis Making. 2006;26:565–74.CrossRef Vickers AJ, Elkin EB. Decision curve analysis: a novel method for evaluating prediction models. Med Decis Making. 2006;26:565–74.CrossRef
24.
go back to reference Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34:2157–64.CrossRef Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34:2157–64.CrossRef
25.
go back to reference Kerr KF, Brown MD, Zhu K, Janes H. Assessing the clinical impact of risk prediction models with decision curves: guidance for correct interpretation and appropriate use. J Clin Oncol. 2016;34:2534–40.CrossRef Kerr KF, Brown MD, Zhu K, Janes H. Assessing the clinical impact of risk prediction models with decision curves: guidance for correct interpretation and appropriate use. J Clin Oncol. 2016;34:2534–40.CrossRef
26.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.CrossRef Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.CrossRef
27.
go back to reference Nelson H, Petrelli N, Carlin A, Couture J, Fleshman J, Guillem J, Miedema B, Ota D, Sargent D. National Cancer institute expert P: guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst. 2001;93:583–96.CrossRef Nelson H, Petrelli N, Carlin A, Couture J, Fleshman J, Guillem J, Miedema B, Ota D, Sargent D. National Cancer institute expert P: guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst. 2001;93:583–96.CrossRef
28.
go back to reference Benson AB, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Engstrom PF, Enzinger PC, Fakih MG, Fenton MJ, et al. Metastatic colon cancer, version 3.2013: featured updates to the NCCN guidelines. J Natl Compr Canc Netw. 2013;11:141–52.CrossRef Benson AB, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Engstrom PF, Enzinger PC, Fakih MG, Fenton MJ, et al. Metastatic colon cancer, version 3.2013: featured updates to the NCCN guidelines. J Natl Compr Canc Netw. 2013;11:141–52.CrossRef
29.
go back to reference Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland JH, Stein KD, Alteri R, Jemal A. Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin. 2016;66:271–89.CrossRef Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland JH, Stein KD, Alteri R, Jemal A. Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin. 2016;66:271–89.CrossRef
30.
go back to reference Enquist IB, Good Z, Jubb AM, Fuh G, Wang X, Junttila MR, Jackson EL, Leong KG. Lymph node-independent liver metastasis in a model of metastatic colorectal cancer. Nat Commun. 2014;5:3530.CrossRef Enquist IB, Good Z, Jubb AM, Fuh G, Wang X, Junttila MR, Jackson EL, Leong KG. Lymph node-independent liver metastasis in a model of metastatic colorectal cancer. Nat Commun. 2014;5:3530.CrossRef
31.
go back to reference Trusolino L, Comoglio PM. Scatter-factor and semaphorin receptors: cell signalling for invasive growth. Nat Rev Cancer. 2002;2:289–300.CrossRef Trusolino L, Comoglio PM. Scatter-factor and semaphorin receptors: cell signalling for invasive growth. Nat Rev Cancer. 2002;2:289–300.CrossRef
32.
go back to reference Takeuchi H, Bilchik A, Saha S, Turner R, Wiese D, Tanaka M, Kuo C, Wang HJ, Hoon DS. c-MET expression level in primary colon cancer: a predictor of tumor invasion and lymph node metastases. Clin Cancer Res. 2003;9:1480–8.PubMed Takeuchi H, Bilchik A, Saha S, Turner R, Wiese D, Tanaka M, Kuo C, Wang HJ, Hoon DS. c-MET expression level in primary colon cancer: a predictor of tumor invasion and lymph node metastases. Clin Cancer Res. 2003;9:1480–8.PubMed
33.
go back to reference Zuo Y, Ren S, Wang M, Liu B, Yang J, Kuai X, Lin C, Zhao D, Tang L, He F. Novel roles of liver sinusoidal endothelial cell lectin in colon carcinoma cell adhesion, migration and in-vivo metastasis to the liver. Gut. 2013;62:1169–78.CrossRef Zuo Y, Ren S, Wang M, Liu B, Yang J, Kuai X, Lin C, Zhao D, Tang L, He F. Novel roles of liver sinusoidal endothelial cell lectin in colon carcinoma cell adhesion, migration and in-vivo metastasis to the liver. Gut. 2013;62:1169–78.CrossRef
34.
go back to reference Choi J, Oh SN, Yeo DM, Kang WK, Jung CK, Kim SW, Park MY. Computed tomography and magnetic resonance imaging evaluation of lymph node metastasis in early colorectal cancer. World J Gastroenterol. 2015;21:556–62.CrossRef Choi J, Oh SN, Yeo DM, Kang WK, Jung CK, Kim SW, Park MY. Computed tomography and magnetic resonance imaging evaluation of lymph node metastasis in early colorectal cancer. World J Gastroenterol. 2015;21:556–62.CrossRef
35.
go back to reference Weiser MR, Landmann RG, Kattan MW, Gonen M, Shia J, Chou J, Paty PB, Guillem JG, Temple LK, Schrag D, et al. Individualized prediction of colon cancer recurrence using a nomogram. J Clin Oncol. 2008;26:380–5.CrossRef Weiser MR, Landmann RG, Kattan MW, Gonen M, Shia J, Chou J, Paty PB, Guillem JG, Temple LK, Schrag D, et al. Individualized prediction of colon cancer recurrence using a nomogram. J Clin Oncol. 2008;26:380–5.CrossRef
Metadata
Title
Novel nomograms to predict lymph node metastasis and liver metastasis in patients with early colon carcinoma
Authors
Yongcong Yan
Haohan Liu
Kai Mao
Mengyu Zhang
Qianlei Zhou
Wei Yu
Bingchao Shi
Jie Wang
Zhiyu Xiao
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-1940-1

Other articles of this Issue 1/2019

Journal of Translational Medicine 1/2019 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.