International Journal of Colorectal Disease

, Volume 34, Issue 3, pp 533–543 | Cite as

Patterns of bone metastases in newly diagnosed colorectal cancer: a real-world analysis in the SEER database

  • Xu Guo
  • Chao Zhang
  • Wenjuan Ma
  • Fei Tian
  • Guijun Xu
  • Xiuxin Han
  • Peng Sun
  • Vladimir P. Baklaushev
  • Andrey S. Bryukhovetskiy
  • Guowen Wang
  • Yulin MaEmail author
  • Xin WangEmail author
Original Article



To investigate the incidence and the associated factors for bone metastases (BM) development and prognosis in initial colorectal cancer (CRC) with a large sample using Surveillance, Epidemiology, and End Results (SEER) cohort.


Primary CRC patients, who were initially diagnosed between 2010 and 2015 in the SEER database, were included to analyze BM incidence and risk factors for BM occurrence. The patients with at least 1-year follow-up were involved to investigate the prognostic factors for BM. Multivariable logistic and proportional hazard regression models were used to investigate the risk factors for BM development and prognosis, respectively.


A total of 212,787 eligible CRC patients were included and 2557 of them were diagnosed with de novo BM (1.20%). Rectal cancer presented significantly higher BM incidence than right and left colon cancer (χ2 = 107.64, P < 0.001). T1 stage, poor differentiated grade, and brain metastases were homogeneously associated factors for BM development and BM patients’ survival. Male gender, higher N stage, rectal site, elevated carcinoembryonic antigen, and lung and liver metastases were positively associated with BM occurrence. Older age, unmarried status, right colon site, and non-surgery were found to positively correlate with the death risk of CRC patients with BM.


BM is rare in CRC patients. Homogeneous and heterogeneous factors were found for BM development and BM patients’ survival. The risk factors and prognostic factors can be used for BM screening and patient’s prognosis estimation.


Bone metastases Colorectal cancer Risk factor Prognosis factor SEER 



The present study was sponsored by the Natural Science Foundation of China (81702161, 81872184, 81801781, and 81602363), the grant of Russian Foundation of Basic Research (15–29-01338), Natural Science Foundation of Tianjin Science and Technology Committee China (17JCQNJC11000), Natural Science Foundation of Tianjin Medical University (2016KYZQ10), and The Doctor Start-up Grant of Tianjin Medical University Cancer Institute and Hospital [B1612, B1711].

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The present study complied with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards and the study was approved by the Research Ethics Board of the Tianjin Medical University Cancer Institute and Hospital.

Informed consent

The SEER database is an open public database, and the release of data from the SEER database does not require informed patient consent because cancer is a reportable disease in every state of the USA.


  1. 1.
    Lyon France: International Agency for Research on Cancer (2013). Available at Accessed 6th July 2018
  2. 2.
    Roth ES, Fetzer DT, Barron BJ, Joseph UA, Gayed IW, Wan DQ (2009) Does colon cancer ever metastasize to bone first? A temporal analysis of colorectal cancer progression. BMC Cancer 9:274Google Scholar
  3. 3.
    Van Cutsem E, Oliveira J (2009) Advanced colorectal cancer: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 20(Suppl):461–463Google Scholar
  4. 4.
    Baek SJ, Hur H, Min BS, Baik SH, Lee KY, Kim NK (2016) The characteristics of bone metastasis in patients with colorectal cancer: a long-term report from a single institution. World J Surg 40(4):982–986CrossRefGoogle Scholar
  5. 5.
    Zhenghong, Zihua Z, Guoweijian, Zhangning, Caiyunyun, Yingjiangshan et al (2017) Retrospective study of predictors of bone metastasis in colorectal cancer patients. J Bone Oncol 9:25–28Google Scholar
  6. 6.
    Abdel-Rahman O (2018) Predictors of skeletal-related events among cancer patients with bone metastases treated with zoledronic acid: a secondary analysis of a randomized study. Expert Opin Drug Saf 17(8):757–761CrossRefGoogle Scholar
  7. 7.
    Hage WD, Aboulafia AJ, Aboulafia DM (2000) Incidence, location, and diagnostic evaluation of metastatic bone disease. Orthop Clin North Am 31(4):515–528CrossRefGoogle Scholar
  8. 8.
    Guo X, Zhang C, Guo Q, Xu Y, Feng G, Li L et al (2018) The homogeneous and heterogeneous risk factors for the morbidity and prognosis of bone metastasis in patients with prostate cancer. Cancer Manag Res 10:1639–1646Google Scholar
  9. 9.
    Khattak MA, Martin HL, Beeke C, Price T, Carruthers S, Kim S et al (2012) Survival differences in patients with metastatic colorectal cancer and with single site metastatic disease at initial presentation: results from south Australian clinical registry for advanced colorectal cancer. Clin Colorectal Cancer 11(4):247–254CrossRefGoogle Scholar
  10. 10.
    Kawamura H, Yamaguchi T, Yano Y, Hozumi T, Takaki Y, Matsumoto H et al (2018) Characteristics and prognostic factors of bone metastasis in patients with colorectal cancer. Dis Colon Rectum 61(6):673–678Google Scholar
  11. 11.
    Cassidy J, Saltz LB, Giantonio BJ, Kabbinavar FF, Hurwitz HI, Rohr UP (2010) Effect of bevacizumab in older patients with metastatic colorectal cancer: pooled analysis of four randomized studies. J Cancer Res Clin Oncol 136(5):737–743CrossRefGoogle Scholar
  12. 12.
    Portales F, Thezenas S, Samalin E, Assenat E, Mazard T, Ychou M (2015) Bone metastases in gastrointestinal cancer. Clin Exp Metastasis 32(1):7–14CrossRefGoogle Scholar
  13. 13.
    Li A, Tan Z, Fu C, Wang H, Yuan J (2017) Analysis of risk factors for bone metastasis after radical resection of colorectal cancer within 5 years. Zhonghua Wei Chang Wai Ke Za Zhi 20(1):58–61Google Scholar
  14. 14.
    Sun C, Deng Y, Zhou H, Hu ZQ (2015) Risk factors for the development of metachronous bone metastasis in colorectal cancer patients after curative resection. Int J Surg 21:145–149Google Scholar
  15. 15.
    Liu F, Zhao J, Xie J, Xie L, Zhu J, Cai S, Zheng H, Xu Y (2016) Prognostic risk factors in patients with bone metastasis from colorectal cancer. In: Tumour Biol, vol 37, pp 16127–16134Google Scholar
  16. 16.
    Heras P, Karagiannis S, Kritikos K, Hatzopoulos A, Mitsibounas D (2007) Ibandronate is effective in preventing skeletal events in patients with bone metastases from colorectal cancer. Eur J Cancer Care (Engl) 16(6):539–542CrossRefGoogle Scholar
  17. 17.
    Zhang Y, Guo X, Wang G, Ma W, Liu R, Han X et al (2018) Real-world study of the incidence, risk factors, and prognostic factors associated with bone metastases in women with uterine cervical cancer using Surveillance, Epidemiology, and End Results (SEER) data analysis. Med Sci Monit 24:6387–6397Google Scholar
  18. 18.
    Xiong Z, Deng G, Huang X, Li X, Xie X, Wang J et al (2018) Bone metastasis pattern in initial metastatic breast cancer: a population-based study. Cancer Manag Res 10:287–295Google Scholar
  19. 19.
    Santini D, Tampellini M, Vincenzi B, Ibrahim T, Ortega C, Virzi V, Silvestris N, Berardi R, Masini C, Calipari N, Ottaviani D, Catalano V, Badalamenti G, Giannicola R, Fabbri F, Venditti O, Fratto ME, Mazzara C, Latiano TP, Bertolini F, Petrelli F, Ottone A, Caroti C, Salvatore L, Falcone A, Giordani P, Addeo R, Aglietta M, Cascinu S, Barni S, Maiello E, Tonini G (2012) Natural history of bone metastasis in colorectal cancer: final results of a large Italian bone metastases study. Ann Oncol 23(8):2072–2077CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Bone and Soft Tissue Tumors, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin’s Clinical Research Center for CancerTianjin Medical University Cancer Institute and HospitalTianjinChina
  2. 2.Department of OrthopedicsCangzhou Central HospitalCangzhouChina
  3. 3.Department of Breast Imaging, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin’s Clinical Research Center for CancerTianjin Medical University Cancer Institute and HospitalTianjinChina
  4. 4.Department of colorectal cancer, National Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin’s Clinical Research Center for CancerTianjin Medical University Cancer Institute and HospitalTianjinChina
  5. 5.Department of General SurgeryThe Second Affiliated Hospital of Harbin Medical University Harbin, ChinaHarbinChina
  6. 6.Department of Colorectal Surgery, National Cancer CenterChinese Academy of Medical Sciences and Peking Union Medical CollegeBeijingChina
  7. 7.Federal Research and Clinical Center of Specialized Medical Care and Medical Technologies, Federal Biomedical Agency of the Russian FederationMoscowRussian Federation
  8. 8.Department of Epidemiology and Biostatistics, First Affiliated HospitalArmy Medical UniversityChongqingChina

Personalised recommendations