{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T14:33:32Z","timestamp":1772030012765,"version":"3.50.1"},"reference-count":50,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T00:00:00Z","timestamp":1771977600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: Colorectal cancer is a significant global health burden, with lung metastasis contributing substantially to mortality. Accurate risk stratification of synchronous lung metastasis (sLM) in patients with T1 colorectal cancer is important for informing staging decisions, yet no validated tool exists to guide selective chest computed tomography (CT) in this population. This study aimed to develop and validate two complementary nomograms: a clinicopathologic model (Model A) for pre-imaging risk stratification to guide chest CT decisions, and a post-staging model (Model B) incorporating concurrent organ metastasis status for comprehensive risk profiling. Materials and Methods: We utilized data from the Surveillance, Epidemiology, and End Results database, including patients diagnosed with T1 colorectal cancer between 2010 and 2020. Logistic regression analyses identified significant predictors of synchronous lung metastasis. A nomogram was constructed based on these predictors and validated using a split-sample approach. Results: The study included 41,728 patients with T1 colorectal cancer. Significant predictors of synchronous lung metastasis included tumor grade, size, location, lymph node involvement, and concurrent metastases in other organs. Two models were developed: Model A (clinicopathologic-only) demonstrated moderate discriminatory ability (AUC = 0.728, 95% CI: 0.710\u20130.746), while Model B (including concurrent organ metastasis status) demonstrated good discrimination (AUC = 0.856, 95% CI: 0.843\u20130.869): Model A validation AUC = 0.716; Model B validation AUC = 0.849. Calibration plots showed good agreement between predicted and observed probabilities of synchronous lung metastasis. Conclusions: This study developed and internally validated two nomograms for predicting sLM in patients with T1 CRC. Model A, using readily available clinicopathological factors, may support selective chest CT decisions during initial staging. Model B, incorporating post-staging information, may assist in prognostic counseling. External validation is required before clinical implementation.<\/jats:p>","DOI":"10.3390\/medicina62030431","type":"journal-article","created":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T12:35:17Z","timestamp":1772022917000},"page":"431","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Nomogram Development for Predicting Synchronous Lung Metastasis in Patients with T1 Colorectal Cancer: An SEER-Based Analysis"],"prefix":"10.3390","volume":"62","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5764-1736","authenticated-orcid":false,"given":"Pin-Chun","family":"Chen","sequence":"first","affiliation":[{"name":"Division of Colon and Rectal Surgery, Department of Surgery, E-DA Hospital, I-Shou University, Kaohsiung 824, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6399-7712","authenticated-orcid":false,"given":"Yi-Kai","family":"Kao","sequence":"additional","affiliation":[{"name":"Division of Colon and Rectal Surgery, Department of Surgery, E-DA Hospital, I-Shou University, Kaohsiung 824, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Po-Wen","family":"Yang","sequence":"additional","affiliation":[{"name":"Division of Colon and Rectal Surgery, Department of Surgery, E-DA Hospital, I-Shou University, Kaohsiung 824, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chia-Hung","family":"Chen","sequence":"additional","affiliation":[{"name":"Division of Colon and Rectal Surgery, Department of Surgery, E-DA Hospital, I-Shou University, Kaohsiung 824, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5311-6889","authenticated-orcid":false,"given":"Chih-I","family":"Chen","sequence":"additional","affiliation":[{"name":"Division of Colon and Rectal Surgery, Department of Surgery, E-DA Hospital, I-Shou University, Kaohsiung 824, Taiwan"},{"name":"College of Management, National Sun Yat-sen University, Kaohsiung 804, Taiwan"},{"name":"School of Medicine, I-Shou University, Kaohsiung 824, Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2026,2,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"55","DOI":"10.2147\/CLEP.S388323","article-title":"Temporal trends in the disease burden of colorectal cancer with its risk factors at the global and national level from 1990 to 2019, and projections until 2044","volume":"15","author":"Liu","year":"2023","journal-title":"Clin. Epidemiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1136\/gutjnl-2022-327736","article-title":"Global burden of colorectal cancer in 2020 and 2040: Incidence and mortality estimates from GLOBOCAN","volume":"72","author":"Morgan","year":"2023","journal-title":"Gut"},{"key":"ref_3","first-page":"17","article-title":"Cancer statistics, 2023","volume":"73","author":"Siegel","year":"2023","journal-title":"CA Cancer J. Clin."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Filip, S., Vymetalkova, V., Petera, J., Vodickova, L., Kubecek, O., John, S., Cecka, F., Krupova, M., Manethova, M., and Cervena, K. (2020). Distant metastasis in colorectal cancer patients\u2014Do we have new predicting clinicopathological and molecular biomarkers? A comprehensive review. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21155255"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"38658","DOI":"10.18632\/oncotarget.6130","article-title":"Pattern of distant metastases in colorectal cancer: A SEER based study","volume":"6","author":"Qiu","year":"2015","journal-title":"Oncotarget"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1186\/s12957-021-02140-6","article-title":"Nomogram based on homogeneous and heterogeneous associated factors for predicting distant metastases in patients with colorectal cancer","volume":"19","author":"Luo","year":"2021","journal-title":"World J. Surg. Oncol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Wang, H., Shan, X., Zhang, M., Qian, K., Shen, Z., and Zhou, W. (2022). Homogeneous and heterogeneous risk and prognostic factors for lung metastasis in colorectal cancer patients. BMC Gastroenterol., 22.","DOI":"10.1186\/s12876-022-02270-5"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1007\/s00384-019-03270-w","article-title":"Pulmonary metastasis in newly diagnosed colon-rectal cancer: A population-based nomogram study","volume":"34","author":"Huang","year":"2019","journal-title":"Int. J. Color. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Steenhuis, E.G.M., Schoenaker, I.J.H., De Groot, J.W.B., Stigt, J.A., Reerink, O., De Vos tot Nederveen Cappel, W.H., Westreenen Van, H.L., and Brohet, R.M. (2022). High Yield of Chest X-ray in the Follow-Up of Colorectal Cancer. J. Clin. Med., 11.","DOI":"10.3390\/jcm11133828"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"6131485","DOI":"10.1155\/2020\/6131485","article-title":"Predictive and Prognostic Factors of Synchronous Colorectal Lung-Limited Metastasis","volume":"2020","author":"Li","year":"2020","journal-title":"Gastroenterol. Res. Pract."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1007\/s12029-019-00325-7","article-title":"Predictive nomograms for synchronous liver and lung metastasis in colon cancer","volume":"51","author":"Gaitanidis","year":"2020","journal-title":"J. Gastrointest. Cancer"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Wang, S., Chen, L., Feng, Y., Swinnen, J.V., Jonscher, C., Van Ongeval, C., and Ni, Y. (2022). Heterogeneity of synchronous lung metastasis calls for risk stratification and prognostic classification: Evidence from a population-based database. Cancers, 14.","DOI":"10.3390\/cancers14071608"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"S259","DOI":"10.1097\/01.XCS.0000895044.14453.8d","article-title":"Do resected colorectal cancer patients need early chest imaging? Impact of clinicopathologic characteristics on time to development of pulmonary metastases","volume":"235","author":"Deboever","year":"2022","journal-title":"J. Am. Coll. Surg."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1186\/s13045-022-01225-3","article-title":"Development of a novel combined nomogram model integrating deep learning-pathomics, radiomics and immunoscore to predict postoperative outcome of colorectal cancer lung metastasis patients","volume":"15","author":"Wang","year":"2022","journal-title":"J. Hematol. Oncol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1080\/13645706.2024.2404046","article-title":"Can we apply the concept of sentinel lymph nodes in rectal cancer surgery?","volume":"33","author":"Ammirati","year":"2024","journal-title":"Minim. Invasive Ther. Allied Technol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1002\/ctm2.30","article-title":"Development and external validation of a predictive scoring system associated with metastasis of T1-2 colorectal tumors to lymph nodes","volume":"10","author":"Mo","year":"2020","journal-title":"Clin. Transl. Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1007\/s00384-020-03722-8","article-title":"Nomogram for predicting occurrence and prognosis of liver metastasis in colorectal cancer: A population-based study","volume":"36","author":"Tang","year":"2021","journal-title":"Int. J. Color. Dis."},{"key":"ref_18","unstructured":"National Cancer Institute (2022). SEER* Explorer: An Interactive Website for SEER Cancer Statistics, National Cancer Institute. Surveillance Research Program."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"14057","DOI":"10.1007\/s00432-023-05221-z","article-title":"Developing prognostic nomograms to predict overall survival and cancer-specific survival in synchronous multiple primary colorectal cancer based on the SEER database","volume":"149","author":"Zhang","year":"2023","journal-title":"J. Cancer Res. Clin. Oncol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1007\/s00384-023-04435-4","article-title":"A novel risk prediction nomogram for early death in patients with resected synchronous multiple primary colorectal cancer based on the SEER database","volume":"38","author":"Zhang","year":"2023","journal-title":"Int. J. Color. Dis."},{"key":"ref_21","first-page":"6","article-title":"Molecular heterogeneity in colorectal cancer: Insights from genetic profiling","volume":"3","author":"Younis","year":"2021","journal-title":"J. Adv. Appl. Sci. Res."},{"key":"ref_22","first-page":"107","article-title":"Molecular stratification of colorectal cancer","volume":"522","year":"2015","journal-title":"Rad Hrvat. Akad. Znan. Umjet. Med. Znan."},{"key":"ref_23","first-page":"81","article-title":"Molecular Stratification of Colorectal Cancer: Moving from the Laboratory to Clinical Practice","volume":"13","author":"Davidson","year":"2017","journal-title":"Curr. Color. Cancer Rep."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Seligmann, J.F., and Seymour, M.T. (2017). Use of Gene Expression Profiles to Distinguish Molecular Subtypes in Colorectal Cancer: Progression Toward Primetime, Oxford University Press.","DOI":"10.1093\/jnci\/djx019"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"29765","DOI":"10.1038\/srep29765","article-title":"Patterns of metastasis in colon and rectal cancer","volume":"6","author":"Hemminki","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_26","first-page":"463","article-title":"Analysis of risk factors for pulmonary metastasis after curative resection of colorectal cancer","volume":"16","author":"Zhang","year":"2013","journal-title":"Zhonghua Wei Chang Wai Ke Za Zhi Chin. J. Gastrointest. Surg."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1111\/his.14128","article-title":"Poorly differentiated clusters in colorectal cancer: A current review and implications for future practice","volume":"77","author":"Shivji","year":"2020","journal-title":"Histopathology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2230079","DOI":"10.1155\/2022\/2230079","article-title":"Imaging Characteristics and Prognostic Value of Isolated Pulmonary Metastasis from Colorectal Cancer Demonstrated with18F-FDG PET\/CT","volume":"2022","author":"Yu","year":"2022","journal-title":"BioMed Res. Int."},{"key":"ref_29","first-page":"3463","article-title":"Clinicopathological study of poorly differentiated colorectal adenocarcinomas: Comparison between solid-type and non-solid-type adenocarcinomas","volume":"31","author":"Komori","year":"2011","journal-title":"Anticancer Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"7318","DOI":"10.1158\/1078-0432.CCR-04-0485","article-title":"High expression of PRL-3 promotes cancer cell motility and liver metastasis in human colorectal cancer: A predictive molecular marker of metachronous liver and lung metastases","volume":"10","author":"Kato","year":"2004","journal-title":"Clin. Cancer Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1016\/S1010-7940(01)00724-2","article-title":"Survival, disease-free interval, and associated tumor features in patients with colon\/rectal carcinomas and their resected intra-pulmonary metastases","volume":"19","author":"Zink","year":"2001","journal-title":"Eur. J. Cardio-Thorac. Surg."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1093\/icvts\/ivw273","article-title":"Are there recognized prognostic factors for patients undergoing pulmonary metastasectomy for colorectal carcinoma?","volume":"23","author":"Tsitsias","year":"2016","journal-title":"Interact. Cardiovasc. Thorac. Surg."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1007\/s13304-023-01533-4","article-title":"Prognostic impact of tumor size on patients with metastatic colorectal cancer: A large SEER-based retrospective cohort study","volume":"75","author":"Zhang","year":"2023","journal-title":"Updates Surg."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1111\/his.14970","article-title":"Pathological features associated with metastasis in patients with early invasive (pT1) colorectal carcinoma in colorectal polyps","volume":"83","author":"Brown","year":"2023","journal-title":"Histopathology"},{"key":"ref_35","first-page":"492","article-title":"Progress in evaluating the risk of lymph node metastasis in early colorectal cancer","volume":"26","author":"Zhou","year":"2023","journal-title":"Zhonghua Wei Chang Wai Ke Za Zhi Chin. J. Gastrointest. Surg."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Aridi, T., El-Kurdi, A., Khoueiry, P., Fakhruddin, N., Mahfouz, R., and Zaatari, G. (2022). Detection of Genetic Markers Involved in Metastatic Colorectal Carcinoma to Lymph Nodes. Preprint.","DOI":"10.21203\/rs.3.rs-1988504\/v1"},{"key":"ref_37","first-page":"e39735","article-title":"Primary Colorectal Tumor Location and Predictors for Metastasis to the Brain","volume":"15","author":"Franceschi","year":"2023","journal-title":"Cureus"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Liu, L.-L., Sun, J.-D., and Xiang, Z.-L. (2022). Survival nomograms for colorectal carcinoma patients with lung metastasis and lung-only metastasis, based on the SEER database and a single-center external validation cohort. BMC Gastroenterol., 22.","DOI":"10.1186\/s12876-022-02547-9"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1919","DOI":"10.1002\/ijc.33364","article-title":"Patients with colorectal cancer and brain metastasis: The relevance of extracranial metastatic patterns predicting time intervals to first occurrence of intracranial metastasis and survival","volume":"148","author":"Thurmaier","year":"2021","journal-title":"Int. J. Cancer"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1146\/annurev-cancerbio-041916-064715","article-title":"Determinants of organotropic metastasis","volume":"1","author":"Smith","year":"2017","journal-title":"Annu. Rev. Cancer Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"7407190","DOI":"10.1155\/2019\/7407190","article-title":"Mechanisms of metastasis in colorectal cancer and metastatic organotropism: Hematogenous versus peritoneal spread","volume":"2019","author":"Pretzsch","year":"2019","journal-title":"J. Oncol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Snow, T., Snider, J., Comment, L., Stergiopoulos, S., Fisher, V., McCusker, M., and Cho-Phan, C. (2023). Comparison of population characteristics in real-world clinical oncology databases in the US: Flatiron health-foundation medicine clinico-genomic databases, flatiron health research databases, and the national cancer institute SEER population-based cancer registry. medRxiv.","DOI":"10.1101\/2023.01.03.22283682"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1001\/jamasurg.2018.0501","article-title":"Practical guide to surgical data sets: Surveillance, epidemiology, and end results (SEER) database","volume":"153","author":"Doll","year":"2018","journal-title":"JAMA Surg."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1093\/aje\/kwab299","article-title":"Use of linked databases for improved confounding control: Considerations for potential selection bias","volume":"191","author":"Sun","year":"2022","journal-title":"Am. J. Epidemiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"9","DOI":"10.25259\/IHOPEJO_3_2021","article-title":"Sample size and its evolution in research","volume":"1","author":"Gumpili","year":"2022","journal-title":"IHOPE J. Ophthalmol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1007\/s00104-018-0742-y","article-title":"Influence of primary lymph node status of colorectal cancer on the development of pulmonary metastases and thoracic lymph node metastases","volume":"90","author":"Hofmann","year":"2019","journal-title":"Die Chir."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"5178750","DOI":"10.1155\/2023\/5178750","article-title":"Development and Interpretation of a Clinicopathological-Based Model for the Identification of Microsatellite Instability in Colorectal Cancer","volume":"2023","author":"Jiang","year":"2023","journal-title":"Dis. Markers"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1177\/1536867X211025836","article-title":"Bootstrap internal validation command for predictive logistic regression models","volume":"21","author":"Muriel","year":"2021","journal-title":"Stata J."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Khan, S.A., and Rana, Z.A. (2019). Evaluating performance of software defect prediction models using area under precision-Recall curve (AUC-PR). 2019 2nd International Conference on Advancements in Computational Sciences (ICACS), IEEE.","DOI":"10.23919\/ICACS.2019.8689135"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1080\/13645706.2025.2540482","article-title":"Protocol for CLASSICA software as medical device trial","volume":"34","author":"Boland","year":"2025","journal-title":"Minim. Invasive Ther. Allied Technol."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/62\/3\/431\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T13:17:30Z","timestamp":1772025450000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/62\/3\/431"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,25]]},"references-count":50,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2026,3]]}},"alternative-id":["medicina62030431"],"URL":"https:\/\/doi.org\/10.3390\/medicina62030431","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,25]]}}}