{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T01:48:09Z","timestamp":1772070489408,"version":"3.50.1"},"reference-count":54,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,3,22]],"date-time":"2022-03-22T00:00:00Z","timestamp":1647907200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>The epidemiology and associated potential heterogeneity of synchronous lung metastasis (sLM) have not been reported at a population-based level. Cancer patients with valid information about sLM status in the Surveillance, Epidemiology, and End Results database were enrolled. The prevalence of sLM, with a 95% confidential interval, and median survival of sLM, with interquartile range, were calculated and compared by Chi-square analyses and log-rank tests by primary cancer type and clinicopathological factors. Furthermore, the risk factors of sLM development were identified by multivariate logistic regression. Among 1,672,265 enrolled cases, 3.3% cases were identified with sLM, with a median survival of 7 months. Heterogeneity in prevalence and prognosis in sLM was observed among different primary cancers, with the highest prevalence in main bronchus cancer and best survival in testis cancer. Higher prevalence and poorer prognosis were observed in the older population, male population, African American, patients with lower socioeconomic status, and cases with advanced T stage, N stage, or more malignant pathological characteristics. Race, age, T stage, N stage, metastasis to other sites, insurance status and marital status were associated with sLM development (p &lt; 0.001). The current study highlights the heterogeneity of the prevalence and prognosis in patients with sLM.<\/jats:p>","DOI":"10.3390\/cancers14071608","type":"journal-article","created":{"date-parts":[[2022,3,22]],"date-time":"2022-03-22T14:55:35Z","timestamp":1647960935000},"page":"1608","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Heterogeneity of Synchronous Lung Metastasis Calls for Risk Stratification and Prognostic Classification: Evidence from a Population-Based Database"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0656-2760","authenticated-orcid":false,"given":"Shuncong","family":"Wang","sequence":"first","affiliation":[{"name":"Theragnostic Laboratory, KU Leuven, Biomedical Group, Campus Gasthuisberg, 3000 Leuven, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8620-6186","authenticated-orcid":false,"given":"Lei","family":"Chen","sequence":"additional","affiliation":[{"name":"Theragnostic Laboratory, KU Leuven, Biomedical Group, Campus Gasthuisberg, 3000 Leuven, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuanbo","family":"Feng","sequence":"additional","affiliation":[{"name":"Theragnostic Laboratory, KU Leuven, Biomedical Group, Campus Gasthuisberg, 3000 Leuven, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7720-5077","authenticated-orcid":false,"given":"Johan V.","family":"Swinnen","sequence":"additional","affiliation":[{"name":"Laboratory of Lipid Metabolism and Cancer, KU Leuven, Biomedical Group, Campus Gasthuisberg, 3000 Leuven, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Charles","family":"Jonscher","sequence":"additional","affiliation":[{"name":"Institute for Health Metrics & Evaluation, University of Washington, Seattle, WA 98195, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chantal","family":"Van Ongeval","sequence":"additional","affiliation":[{"name":"Department of Radiology, UZ Gasthuisberg, Herestraat 49, 3000 Leuven, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8553-7565","authenticated-orcid":false,"given":"Yicheng","family":"Ni","sequence":"additional","affiliation":[{"name":"Theragnostic Laboratory, KU Leuven, Biomedical Group, Campus Gasthuisberg, 3000 Leuven, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"394","DOI":"10.3322\/caac.21492","article-title":"Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"68","author":"Bray","year":"2018","journal-title":"CA Cancer J. Clin."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1126\/science.1203543","article-title":"A perspective on cancer cell metastasis","volume":"331","author":"Chaffer","year":"2011","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Wang, S., Liu, Y., Feng, Y., Zhang, J., Swinnen, J., Li, Y., and Ni, Y. (2019). A Review on Curability of Cancers: More Efforts for Novel Therapeutic Options Are Needed. Cancers, 11.","DOI":"10.3390\/cancers11111782"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e1006","DOI":"10.1097\/MAO.0000000000002391","article-title":"Predictors of Distant Metastasis and Survival in Adenoid Cystic Carcinoma of the External Auditory Canal","volume":"40","author":"Zhang","year":"2019","journal-title":"Otol. Neurotol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5534","DOI":"10.1002\/cam4.1697","article-title":"Clinical landscape of cancer metastases","volume":"7","author":"Thomsen","year":"2018","journal-title":"Cancer Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1038\/s41556-019-0404-4","article-title":"Tumour exosomal CEMIP protein promotes cancer cell colonization in brain metastasis","volume":"21","author":"Rodrigues","year":"2019","journal-title":"Nat. Cell Biol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Zhang, X., Song, J., Liu, P., Mazid, M.A., Lu, L., Shang, Y., Wei, Y., Gong, P., and Ma, L. (2018). A modified M-stage classification based on the metastatic patterns of pancreatic neuroendocrine neoplasms: A population-based study. BMC Endocr. Disord., 18.","DOI":"10.1186\/s12902-018-0301-z"},{"key":"ref_8","first-page":"1477","article-title":"Incidence and prognosis of liver metastasis at diagnosis: A pan-cancer population-based study","volume":"10","author":"Wang","year":"2020","journal-title":"Am. J. Cancer Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1038\/nrclinonc.2014.96","article-title":"The oligometastatic state\u2014Separating truth from wishful thinking","volume":"11","author":"Palma","year":"2014","journal-title":"Nat. Rev. Clin. Oncol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"922","DOI":"10.1002\/cam4.1370","article-title":"Risk factors and survival outcomes in patients with breast cancer and lung metastasis: A population-based study","volume":"7","author":"Xiao","year":"2018","journal-title":"Cancer Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1007\/s00384-019-03434-8","article-title":"Incidence and prognosis of pulmonary metastasis in colorectal cancer: A population-based study","volume":"35","author":"Ge","year":"2020","journal-title":"Int. J. Colorectal Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"78","DOI":"10.3322\/canjclin.54.2.78","article-title":"Cancer disparities by race\/ethnicity and socioeconomic status","volume":"54","author":"Ward","year":"2004","journal-title":"CA Cancer J. Clin."},{"key":"ref_13","unstructured":"SEER Database (2022, February 01). Available online: https:\/\/seer.cancer.gov\/."},{"key":"ref_14","unstructured":"SEER (2021, November 19). ICD-O-3 Coding Materials, Available online: https:\/\/seer.cancer.gov\/icd-o-3\/."},{"key":"ref_15","unstructured":"SEER (2022, February 28). Appendix C: Site Specific Coding Modules, Available online: https:\/\/seer.cancer.gov\/archive\/manuals\/2021\/appendixc.html?&url=\/manuals\/2021\/appendixc.html."},{"key":"ref_16","unstructured":"SEER Database (2021, November 19). Race Recode Changes, Available online: https:\/\/seer.cancer.gov\/seerstat\/variables\/seer\/race_ethnicity\/."},{"key":"ref_17","unstructured":"(2021, November 19). AJCC Staging System. Available online: https:\/\/www.facs.org\/quality-programs\/cancer\/ajcc."},{"key":"ref_18","unstructured":"(2021, June 22). A Confidence Interval for A Population Proportion. Available online: https:\/\/openstax.org\/books\/introductory-business-statistics\/pages\/8-3-a-confidence-interval-for-a-population-proportion."},{"key":"ref_19","unstructured":"USDA (2021, November 19). Available online: https:\/\/www.usda.gov\/."},{"key":"ref_20","unstructured":"Kassambara, A., Kosinski, M., Biecek, P., Fabian, S., and Survminer: Drawing Survival Curves Using \u2018ggplot2\u2019 (2021, November 19). R Package Version 0.4.4. Available online: https:\/\/rpkgs.datanovia.com\/survminer\/."},{"key":"ref_21","unstructured":"Therneau, T., and A Package for Survival Analysis in R (2021, November 19). R Package Version 3.2-7. Available online: https:\/\/cran.r-project.org\/web\/packages\/survival\/vignettes\/survival.pdf."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2707","DOI":"10.1158\/1055-9965.EPI-08-0232","article-title":"Cigarette smoking and risk of lung metastasis from esophageal cancer","volume":"17","author":"Abrams","year":"2008","journal-title":"Cancer Epidemiol. Biomark. Prev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"O322","DOI":"10.1111\/codi.13833","article-title":"Smoking is a risk factor for pulmonary metastasis in colorectal cancer","volume":"19","author":"Yahagi","year":"2017","journal-title":"Colorectal Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"9623","DOI":"10.2147\/OTT.S263250","article-title":"The Impact of Smoking on Pulmonary Metastasis in Colorectal Cancer","volume":"13","author":"Makino","year":"2020","journal-title":"Onco Targets Ther."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"936","DOI":"10.4049\/jimmunol.178.2.936","article-title":"Cigarette smoke impairs NK cell-dependent tumor immune surveillance","volume":"178","author":"Lu","year":"2007","journal-title":"J. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1635","DOI":"10.1378\/chest.119.6.1635","article-title":"Cigarette smoking and the risk of pulmonary metastasis from breast cancer","volume":"119","author":"Murin","year":"2001","journal-title":"Chest"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1467","DOI":"10.1378\/chest.125.4.1467","article-title":"The effect of cigarette smoke exposure on pulmonary metastatic disease in a murine model of metastatic breast cancer","volume":"125","author":"Murin","year":"2004","journal-title":"Chest"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"789","DOI":"10.4161\/cbt.28552","article-title":"Systemic inflammation promotes lung metastasis via E-selectin upregulation in mouse breast cancer model","volume":"15","author":"Jiang","year":"2014","journal-title":"Cancer Biol. Ther."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1158\/1541-7786.MCR-07-0309","article-title":"Host nuclear factor-kappaB activation potentiates lung cancer metastasis","volume":"6","author":"Stathopoulos","year":"2008","journal-title":"Mol. Cancer Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.canlet.2020.08.010","article-title":"E-cigarette promotes breast carcinoma progression and lung metastasis: Macrophage-tumor cells crosstalk and the role of CCL5 and VCAM-1","volume":"491","author":"Pham","year":"2020","journal-title":"Cancer Lett."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"45","DOI":"10.2217\/fon-2019-0053","article-title":"Precision treatment of post pneumonectomy unilateral laryngeal paralysis due to cancer","volume":"16","author":"Cocuzza","year":"2020","journal-title":"Future Oncol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.anl.2021.05.007","article-title":"Neck dissection and trans oral robotic surgery for oropharyngeal squamous cell carcinoma","volume":"49","author":"Meccariello","year":"2022","journal-title":"Auris Nasus Larynx"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"6073","DOI":"10.1158\/0008-5472.CAN-18-0136","article-title":"HER2\/EGFR-AKT Signaling Switches TGF\u03b2 from Inhibiting Cell Proliferation to Promoting Cell Migration in Breast Cancer","volume":"78","author":"Huang","year":"2018","journal-title":"Cancer Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"3153","DOI":"10.1200\/JCO.2007.15.5986","article-title":"Prognostic significance of Nottingham histologic grade in invasive breast carcinoma","volume":"26","author":"Rakha","year":"2008","journal-title":"J. Clin. Oncol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.canlet.2019.01.023","article-title":"RLIP inhibition suppresses breast-to-lung metastasis","volume":"447","author":"Singhal","year":"2019","journal-title":"Cancer Lett."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1111\/jcmm.12745","article-title":"Alpha fetoprotein plays a critical role in promoting metastasis of hepatocellular carcinoma cells","volume":"20","author":"Lu","year":"2016","journal-title":"J. Cell. Mol. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"5812","DOI":"10.7150\/jca.46927","article-title":"Differences in tumour characteristics of Hepatocellular Carcinoma between patients with and without Cirrhosis: A population-based study","volume":"11","author":"Yan","year":"2020","journal-title":"J. Cancer"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Engstrand, J., Nilsson, H., Str\u00f6mberg, C., Jonas, E., and Freedman, J. (2018). Colorectal cancer liver metastases\u2014A population-based study on incidence, management and survival. BMC Cancer, 18.","DOI":"10.1186\/s12885-017-3925-x"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1038\/bjc.2014.619","article-title":"Association between KRAS mutation and lung metastasis in advanced colorectal cancer","volume":"112","author":"Pereira","year":"2015","journal-title":"Br. J. Cancer"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Kim, M.-J., Lee, H.S., Kim, J.H., Kim, Y.J., Kwon, J.H., Lee, J.-O., Bang, S.-M., Park, K.U., Kim, D.-W., and Kang, S.-B. (2012). Different metastatic pattern according to the KRAS mutational status and site-specific discordance of KRAS status in patients with colorectal cancer. BMC Cancer, 12.","DOI":"10.1186\/1471-2407-12-347"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.1093\/neuonc\/nox077","article-title":"Incidence and prognosis of patients with brain metastases at diagnosis of systemic malignancy: A population-based study","volume":"19","author":"Cagney","year":"2017","journal-title":"Neuro Oncol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1038\/s41588-019-0423-x","article-title":"Quantitative evidence for early metastatic seeding in colorectal cancer","volume":"51","author":"Hu","year":"2019","journal-title":"Nat. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3322\/caac.21586","article-title":"Understanding and addressing social determinants to advance cancer health equity in the United States: A blueprint for practice, research, and policy","volume":"70","author":"Alcaraz","year":"2020","journal-title":"CA Cancer J. Clin."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"165","DOI":"10.3322\/caac.21270","article-title":"Inferior cancer outcomes more common for uninsured and Medicaid patients","volume":"65","author":"Barton","year":"2015","journal-title":"CA Cancer J. Clin."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3869","DOI":"10.1200\/JCO.2013.49.6489","article-title":"Marital status and survival in patients with cancer","volume":"31","author":"Aizer","year":"2013","journal-title":"J. Clin. Oncol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"982","DOI":"10.1056\/NEJMms1902657","article-title":"Death by Stereotype? Cancer Treatment in Unmarried Patients","volume":"381","author":"DelFattore","year":"2019","journal-title":"N. Engl. J. Med."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1016\/j.ejso.2018.05.024","article-title":"Socioeconomic differences in selection for liver resection in metastatic colorectal cancer and the impact on survival","volume":"44","author":"Vallance","year":"2018","journal-title":"Eur. J. Surg. Oncol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e1920471","DOI":"10.1001\/jamanetworkopen.2019.20471","article-title":"Trends in the Use of Stereotactic Body Radiotherapy for Treatment of Prostate Cancer in the United States","volume":"3","author":"Mahase","year":"2020","journal-title":"JAMA Netw. Open"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1097\/CJI.0000000000000294","article-title":"Association of Insurance Status With Presentation, Treatment, and Survival in Melanoma in the Era of Immune Checkpoint Inhibitors","volume":"43","author":"Jain","year":"2020","journal-title":"J. Immunother."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1200\/JCO.2017.75.2501","article-title":"Breast Cancer Diagnosis and Treatment After High-Deductible Insurance Enrollment","volume":"36","author":"Wharam","year":"2018","journal-title":"J. Clin. Oncol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"4110","DOI":"10.1200\/JCO.2016.68.5701","article-title":"Impact of Health Insurance Expansion on the Treatment of Colorectal Cancer","volume":"34","author":"Loehrer","year":"2016","journal-title":"J. Clin. Oncol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1186\/s12939-021-01436-z","article-title":"The convergence of racial and income disparities in health insurance coverage in the United States","volume":"20","author":"Lee","year":"2021","journal-title":"Int. J. Equity Health"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"425","DOI":"10.3322\/caac.21494","article-title":"Cancer Statistics for Hispanics\/Latinos, 2018","volume":"68","author":"Miller","year":"2018","journal-title":"CA Cancer J. Clin."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.1111\/j.1525-1497.2003.20807.x","article-title":"Racial and ethnic disparities in cancer screening: The importance of foreign birth as a barrier to care","volume":"18","author":"Goel","year":"2003","journal-title":"J. Gen. Intern. Med."}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/14\/7\/1608\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:41:11Z","timestamp":1760136071000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/14\/7\/1608"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,22]]},"references-count":54,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,4]]}},"alternative-id":["cancers14071608"],"URL":"https:\/\/doi.org\/10.3390\/cancers14071608","relation":{},"ISSN":["2072-6694"],"issn-type":[{"value":"2072-6694","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,22]]}}}