Journal of Cancer Research and Clinical Oncology

, Volume 144, Issue 9, pp 1835–1842 | Cite as

The prognostic value of multiorgan metastases in patients with non-small cell lung cancer and its variants: a SEER-based study

  • Jie Yang
  • Yuan Zhang
  • Xiaoting Sun
  • Aaron M. Gusdon
  • Nan Song
  • Linsong Chen
  • Gening JiangEmail author
  • Yueye HuangEmail author
Original Article – Clinical Oncology



This study aimed to investigate the prognostic value of different organs metastases in patients with non-small cell lung cancer (NSCLC) and its most common subtypes.


We identified 45,423 NSCLC cases (25,129 men and 20,294 women) between 2010 and 2013 with distant metastases, with complete clinical information obtained from the surveillance, epidemiology, and end results (SEER) database.


Bone and liver were the most and the least common metastatic sites with rates of 37.1 and 16.8%, respectively. The mortality rates associated with bone, brain, liver, lung metastases, and multiorgan metastases (MOM) were 73.2, 72.7, 78.3, 65.4, and 77.5%, respectively. Kaplan–Meier analyses demonstrated that patients with MOM and liver metastasis had the worst survival. Compared with NSCLC cases with other organ metastasis, but without the four organs metastasis, hazard ratios (HRs) for lung, bone, brain, and liver metastases, and MOM were 0.906 (95% CI 0.866–0.947), 1.276 (95% CI 1.225–1.330), 1.318 (95% CI 1.260–1.379), 1.481 (95% CI 1.388–1.580), and 1.647 (95% CI 1.587–1.709), respectively. Similar results were obtained for adenocarcinoma (AD) cases.


The mortality risk is highest with MOM and liver metastasis followed by bone, brain, other organ, and lung metastases in NSCLC and AD which is the most common variant for NSCLC. These results will be helpful for pre-treatment evaluation regarding the prognosis of NSCLC patients.


Non-small cell lung cancer Metastasis Prognosis SEER 



We would like to thank all the staff of National Cancer Institute for their efforts toward the SEER program.

Author Contributions

Conception and design: Y.H., J.Y., and G.J.; acquisition, statistical analysis or interpretation of the data: all authors; drafting of the manuscript: Y.H., J.Y., Y.Z. and X.S.; all authors reviewed and approved the final version of the manuscript.


This work was supported by National Natural Science Foundation of China, No. 81600052 (J.Y.) and 81500052 (Y.Z.). This work was also supported by Shanghai Tenth Hospital’s improvement plan for National Natural Science Foundation of China, No. SYGZRPY (Y.H.).

Compliance with ethical standards

Conflict of interest

The authors disclose no potential conflicts of interest related to this study.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study formal consent is waived.

Supplementary material

432_2018_2702_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 20 KB)


  1. Bray F, Jemal A, Grey N, Ferlay J, Forman D (2012) Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol 13:790–801. CrossRefPubMedGoogle Scholar
  2. Brodowicz T, O’Byrne K, Manegold C (2012) Bone matters in lung cancer. Ann Oncol 23:2215–2222. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chang YP et al (2017) The impact of de novo liver metastasis on clinical outcome in patients with advanced non-small-cell lung cancer. PLoS ONE 12:e0178676. CrossRefPubMedPubMedCentralGoogle Scholar
  4. D’Antonio C et al (2014) Bone and brain metastasis in lung cancer: recent advances in therapeutic strategies. Ther Adv Med Oncol 6:101–114. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Detterbeck FC, Boffa DJ, Kim AW, Tanoue LT (2017) The eighth edition lung cancer stage classification. Chest 151:193–203. CrossRefPubMedGoogle Scholar
  6. Eberhardt WE et al (2015) The IASLC lung cancer staging project: proposals for the revision of the M descriptors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol 10:1515–1522. CrossRefPubMedGoogle Scholar
  7. Goldstraw P et al (2007) The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2:706–714. CrossRefPubMedGoogle Scholar
  8. Ichinose Y et al (2000) The prognosis of patients with non-small cell lung cancer found to have carcinomatous pleuritis at thoracotomy. Surg Today 30:1062–1066CrossRefPubMedGoogle Scholar
  9. Iida T et al (2015) Surgical intervention for non-small-cell lung cancer patients with pleural carcinomatosis: results from the Japanese Lung Cancer Registry in 2004. J Thorac Oncol 10:1076–1082. CrossRefPubMedGoogle Scholar
  10. Jett JR, Scott WJ, Rivera MP, Sause WT, American College of Chest P (2003) Guidelines on treatment of stage IIIB non-small cell lung cancer. Chest 123:221S–225SCrossRefPubMedGoogle Scholar
  11. Morgensztern D, Waqar S, Subramanian J, Gao F, Govindan R (2009) Improving survival for stage IV non-small cell lung cancer: a surveillance, epidemiology, and end results survey from 1990 to 2005. J Thorac Oncol 4:1524–1529. CrossRefPubMedGoogle Scholar
  12. Morgensztern D, Ng SH, Gao F, Govindan R (2010) Trends in stage distribution for patients with non-small cell lung cancer: a National Cancer Database survey. J Thorac Oncol 5:29–33. CrossRefPubMedGoogle Scholar
  13. Nakazawa K, Kurishima K, Tamura T, Kagohashi K, Ishikawa H, Satoh H, Hizawa N (2012) Specific organ metastases and survival in small cell lung cancer. Oncol Lett 4:617–620. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ohta Y, Shimizu Y, Matsumoto I, Tamura M, Oda M, Watanabe G (2005) Retrospective review of lung cancer patients with pleural dissemination after limited operations combined with parietal pleurectomy. J Surg Oncol 91:237–242. CrossRefPubMedGoogle Scholar
  15. Rami-Porta R, Asamura H, Travis WD, Rusch VW (2017) Lung cancer—major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin 67:138–155. CrossRefPubMedGoogle Scholar
  16. Ren Y et al (2016) Prognostic effect of liver metastasis in lung cancer patients with distant metastasis. Oncotarget 7:53245–53253. PubMedPubMedCentralCrossRefGoogle Scholar
  17. Riihimaki M, Hemminki A, Fallah M, Thomsen H, Sundquist K, Sundquist J, Hemminki K (2014) Metastatic sites and survival in lung cancer. Lung Cancer 86:78–84. CrossRefPubMedGoogle Scholar
  18. Sanchez de Cos Escuin J et al (2014) Tumor, node and metastasis classification of lung cancer—M1a versus M1b—analysis of M descriptors and other prognostic factors. Lung Cancer 84:182–189. CrossRefPubMedGoogle Scholar
  19. Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67:7–30. CrossRefPubMedGoogle Scholar
  20. Sugiura S, Ando Y, Minami H, Ando M, Sakai S, Shimokata K (1997) Prognostic value of pleural effusion in patients with non-small cell lung cancer. Clin Cancer Res 3:47–50PubMedGoogle Scholar
  21. Sugiura H, Yamada K, Sugiura T, Hida T, Mitsudomi T (2008) Predictors of survival in patients with bone metastasis of lung cancer. Clin Orthop Relat Res 466:729–736. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Tamura T, Kurishima K, Nakazawa K, Kagohashi K, Ishikawa H, Satoh H, Hizawa N (2015) Specific organ metastases and survival in metastatic non-small-cell lung cancer. Mol Clin Oncol 3:217–221. CrossRefPubMedGoogle Scholar
  23. Waqar SN et al (2015) Brain metastases at presentation in patients with non-small cell lung cancer. Am J Clin Oncol 41(1):36–40. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Thoracic Surgery, Shanghai Pulmonary HospitalTongji University School of MedicineShanghaiChina
  2. 2.Department of Respiratory Medicine, Shanghai Pulmonary HospitalTongji University School of MedicineShanghaiChina
  3. 3.Department of Health Services Research & AdministrationUniversity of Nebraska Medical CenterOmahaUSA
  4. 4.Division of Neurocritical Care, Department of NeurologyJohns Hopkins University School of MedicineBaltimoreUSA
  5. 5.Department of Endocrinology and Metabolism, The Center of Thyroid Diseases, The Shanghai Tenth People’s HospitalTongji University School of MedicineShanghaiChina

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