Journal of Gastrointestinal Surgery

, Volume 22, Issue 7, pp 1268–1276 | Cite as

Predictive Nomograms for Synchronous Distant Metastasis in Rectal Cancer

  • Apostolos Gaitanidis
  • Michail Alevizakos
  • Alexandra Tsaroucha
  • Christos Tsalikidis
  • Michail Pitiakoudis
Original Article



Nomograms may be used to quantitatively assess the probability of synchronous distant metastasis. The purpose of this study is to develop predictive nomograms for the presence of synchronous distant metastasis in patients with rectal cancer.


A retrospective analysis of the Surveillance Epidemiology and End Results database was performed for cases diagnosed between 2010 and 2014.


Overall, 46,785 patients with rectal cancer (27,773 [59.4%] males, mean age 63.9 ± 13.7 years) were identified, of which 6192 (13.2%) had liver metastasis, 2767 (5.9%) had lung metastasis, and 601 (1.3%) had bone metastasis. Age, sex, race, tumor location, tumor grade, primary tumor size, CEA levels, perineural invasion, T stage, N stage, and liver and lung metastasis were found to be associated with the presence of synchronous distant metastasis and were included in the predictive models. The c-indexes of these models were 0.99 for liver metastasis, 0.99 for lung metastasis, and 1 for bone metastasis.


Predictive nomograms for the presence of synchronous liver, lung, and bone metastasis were developed and may be used to predict the probability of distant disease in rectal cancer patients.


Rectum Cancer Colorectal cancer Metastasis Liver Lung Bone 


Author Contributions

Conception/Design: Gaitanidis, Alevizakos, Pitiakoudis.

Provision of study material or patients: Gaitanidis, Alevizakos.

Collection and/or assembly of data: Gaitanidis, Alevizakos, Tsaroucha, Tsalikidis.

Data analysis and interpretation: All authors.

Manuscript drafting: Gaitanidis, Alevizakos, Tsalikidis.

Final approval of manuscript: Pitiakoudis.

All authors agree to be accountable for all aspects of this work.


This study was supported by the General Secretariat for Research and Technology (GSRT) and the Hellenic Foundation for Research and Innovation (HFRI).

Compliance with Ethical Standards

Conflicts of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Qiu M, Hu J, Yang D, Cosgrove DP, Xu R. Pattern of distant metastases in colorectal cancer: a SEER based study. Oncotarget. 2015;6(36):38658–38666. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Nordholm-Carstensen A, Krarup P-M, Jorgensen LN, Wille-Jørgensen PA, Harling H. Occurrence and survival of synchronous pulmonary metastases in colorectal cancer: a nationwide cohort study. Eur J Cancer. 2014;50(2):447–456. doi: CrossRefPubMedGoogle Scholar
  3. 3.
    Riihimäki M, Hemminki A, Sundquist J, Hemminki K. Patterns of metastasis in colon and rectal cancer. Sci Rep. 2016;6:29765. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Katoh M, Unakami M, Hara M, Fukuchi S. Bone metastasis from colorectal cancer in autopsy cases. J Gastroenterol. 1995;30(5):615–618. Accessed February 25, 2018.
  5. 5.
    Santini D, Tampellini M, Vincenzi B, et al. Natural history of bone metastasis in colorectal cancer: final results of a large Italian bone metastases study. Ann Oncol. 2012;23(8):2072–2077. doi: CrossRefPubMedGoogle Scholar
  6. 6.
    Hugen N, van de Velde CJH, de Wilt JHW, Nagtegaal ID. Metastatic pattern in colorectal cancer is strongly influenced by histological subtype. Ann Oncol. 2014;25(3):651–657. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Benson AB, Venook AP, Bekaii-Saab T, et al. Rectal Cancer, Version 2.2015. J Natl Compr Canc Netw. 2015;13(6):719–28; quiz 728. Accessed 11, November 2017.CrossRefPubMedGoogle Scholar
  8. 8.
    Glynne-Jones R, Wyrwicz L, Tiret E, et al. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up†. Ann Oncol. 2017;28(suppl_4):iv22-iv40. doi: CrossRefPubMedGoogle Scholar
  9. 9.
    Kirke R, Rajesh A, Verma R, Bankart MJ. Rectal cancer. J Comput Assist Tomogr. 2007;31(4):569–571. doi: CrossRefPubMedGoogle Scholar
  10. 10.
    Hogan J, O’Rourke C, Duff G, et al. Preoperative staging CT thorax in patients with colorectal cancer. Dis Colon rectum. 2014;57(11):1260–1266. doi: CrossRefPubMedGoogle Scholar
  11. 11.
    Nordholm-Carstensen A, Wille-Jørgensen PA, Jorgensen LN, Harling H. Indeterminate pulmonary nodules at colorectal cancer staging: a systematic review of predictive parameters for malignancy. Ann Surg Oncol. 2013;20(12):4022–4030. doi: CrossRefPubMedGoogle Scholar
  12. 12.
    Yongue G, Hotouras A, Murphy J, Mukhtar H, Bhan C, Chan CL. The diagnostic yield of preoperative staging computed tomography of the thorax in colorectal cancer patients without hepatic metastases. Eur J Gastroenterol Hepatol. 2015;27(4):467–470. doi: CrossRefPubMedGoogle Scholar
  13. 13.
    Zhenghong, Zihua Zhu, Guoweijian, et al. Retrospective study of predictors of bone metastasis in colorectal cancer patients. J bone Oncol. 2017;9:25–28. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    National Cancer Institute. Overview of the SEER Program. 2013.
  15. 15.
    Yang D. Build prognostic nomograms for risk assessment using SAS. SAS Glob Forum 2013. 2013;(264):1–7.Google Scholar
  16. 16.
    Iasonos A, Schrag D, Raj G V., Panageas KS. How to build and interpret a nomogram for cancer prognosis. J Clin Oncol. 2008;26(8):1346–1354. doi: CrossRefGoogle Scholar
  17. 17.
    Harrell FE, Lee KL, Califf RM, Pryor DB, Rosati RA. Regression modelling strategies for improved prognostic prediction Stat Med. 3(2):143–152. Accessed 31 July , 2017.
  18. 18.
    Choi DJ, Kwak JM, Kim J, Woo SU, Kim SH. Preoperative chest computerized tomography in patients with locally advanced mid or lower rectal cancer: its role in staging and impact on treatment strategy. J Surg Oncol. 2010;102(6):588–592. doi: CrossRefPubMedGoogle Scholar
  19. 19.
    Kim HY, Lee SJ, Lee G, et al. Should preoperative chest CT be recommended to all colon cancer patients? Ann Surg. 2014;259(2):323–328. doi: CrossRefPubMedGoogle Scholar
  20. 20.
    Restivo A, Zorcolo L, Piga S, Cocco IMF, Casula G. Routine preoperative chest computed tomography does not influence therapeutic strategy in patients with colorectal cancer. Color Dis. 2012;14(5):e216-e221. doi: CrossRefGoogle Scholar
  21. 21.
    Lazzaron AR, Vieira M V., Damin DC. Should preoperative chest computed tomography be performed in all patients with colorectal cancer? Color Dis. 2015;17(10):O184-O190. doi: CrossRefGoogle Scholar
  22. 22.
    Kronawitter U, Kemeny NE, Heelan R, Fata F, Fong Y. Evaluation of chest computed tomography in the staging of patients with potentially resectable liver metastases from colorectal carcinoma. Cancer. 1999;86(2):229–235. Accessed 11 November 2017.CrossRefPubMedGoogle Scholar
  23. 23.
    Nordholm-Carstensen A, Jorgensen LN, Wille-Jørgensen PA, Hansen H, Harling H. Indeterminate pulmonary nodules in colorectal-cancer: do radiologists agree? Ann Surg Oncol. 2015;22(2):543–549. doi: CrossRefPubMedGoogle Scholar
  24. 24.
    McQueen AS, Scott J. CT staging of colorectal cancer: what do you find in the chest? Clin Radiol. 2012;67(4):352–358. doi: CrossRefPubMedGoogle Scholar
  25. 25.
    McCollough CH, Bushberg JT, Fletcher JG, Eckel LJ. Answers to common questions about the use and safety of CT scans. Mayo Clin Proc. 2015;90(10):1380–1392. doi: CrossRefPubMedGoogle Scholar
  26. 26.
    Ono K, Hiraoka T, Ono A, et al. Low-dose CT scan screening for lung cancer: comparison of images and radiation doses between low-dose CT and follow-up standard diagnostic CT. Springerplus. 2013;2:393. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Sun C, Deng Y, Zhou H, Hu ZQ. Risk factors for the development of metachronous bone metastasis in colorectal cancer patients after curative resection. Int J Surg. 2015;21:145–149. doi: CrossRefPubMedGoogle Scholar
  28. 28.
    Li A, Käsmann L, Rades D, Fu C.A Scoring system to predict the development of bone metastasis after radical resection of colorectal cancer. Anticancer Res. 2017;37(9):5169–5172. doi: PubMedGoogle Scholar
  29. 29.
    Roth ES, Fetzer DT, Barron BJ, Joseph UA, Gayed IW, Wan DQ. Does colon cancer ever metastasize to bone first? a temporal analysis of colorectal cancer progression. BMC Cancer. 2009;9:274. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Martin AM, Cagney DN, Catalano PJ, et al. Brain metastases in newly diagnosed breast cancer. JAMA Oncol. 2017;3(8):1069. doi: CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  1. 1.Second Department of Surgery, University General Hospital of AlexandroupoliDemocritus University of Thrace Medical SchoolAlexandroupoliGreece
  2. 2.Department of MedicineUniversity of Pittsburgh Medical CenterPittsburghUSA

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