{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,26]],"date-time":"2026-03-26T09:12:42Z","timestamp":1774516362572,"version":"3.50.1"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,9,28]],"date-time":"2024-09-28T00:00:00Z","timestamp":1727481600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2024,9,28]],"date-time":"2024-09-28T00:00:00Z","timestamp":1727481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/s41598-024-73542-1","type":"journal-article","created":{"date-parts":[[2024,9,28]],"date-time":"2024-09-28T19:02:03Z","timestamp":1727550123000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Precision patient selection for improved detection of circulating genetically abnormal cells in pulmonary nodules"],"prefix":"10.1038","volume":"14","author":[{"given":"Meng","family":"Tu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xinjuan","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hongping","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hongxia","family":"Jia","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yan","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jing","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guojun","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,9,28]]},"reference":[{"key":"73542_CR1","doi-asserted-by":"publisher","first-page":"209","DOI":"10.3322\/caac.21660","volume":"71","author":"H Sung","year":"2021","unstructured":"Sung, H. et al. Global Cancer statistics 2020: GLOBOCAN estimates of incidence and Mortality Worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.71, 209\u2013249. https:\/\/doi.org\/10.3322\/caac.21660 (2021).","journal-title":"CA Cancer J. Clin."},{"key":"73542_CR2","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1016\/S0140-6736(16)30958-8","volume":"389","author":"FR Hirsch","year":"2017","unstructured":"Hirsch, F. R. et al. Lung cancer: Current therapies and new targeted treatments. Lancet. 389, 299\u2013311. https:\/\/doi.org\/10.1016\/S0140-6736(16)30958-8 (2017).","journal-title":"Lancet"},{"key":"73542_CR3","doi-asserted-by":"publisher","first-page":"584","DOI":"10.4065\/83.5.584","volume":"83","author":"JR Molina","year":"2008","unstructured":"Molina, J. R., Yang, P., Cassivi, S. D., Schild, S. E. & Adjei, A. A. Non-small cell lung cancer: Epidemiology, risk factors, treatment, and survivorship. Mayo Clin. Proc.83, 584\u2013594. https:\/\/doi.org\/10.4065\/83.5.584 (2008).","journal-title":"Mayo Clin. Proc."},{"key":"73542_CR4","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.jtho.2015.09.009","volume":"11","author":"P Goldstraw","year":"2016","unstructured":"Goldstraw, P. et al. The IASLC Lung Cancer Staging Project: Proposals for revision of the TNM Stage groupings in the Forthcoming (Eighth) Edition of the TNM classification for Lung Cancer. J. Thorac. Oncol.11, 39\u201351. https:\/\/doi.org\/10.1016\/j.jtho.2015.09.009 (2016).","journal-title":"J. Thorac. Oncol."},{"key":"73542_CR5","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1002\/cncy.22278","volume":"128","author":"RL Katz","year":"2020","unstructured":"Katz, R. L. et al. Identification of circulating tumor cells using 4-color fluorescence in situ hybridization: Validation of a noninvasive aid for ruling out lung cancer in patients with low-dose computed tomography-detected lung nodules. Cancer Cytopathol.128, 553\u2013562. https:\/\/doi.org\/10.1002\/cncy.22278 (2020).","journal-title":"Cancer Cytopathol."},{"key":"73542_CR6","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.1002\/ijc.32486","volume":"146","author":"N Becker","year":"2020","unstructured":"Becker, N. et al. Lung cancer mortality reduction by LDCT screening-results from the randomized German LUSI trial. Int. J. Cancer. 146, 1503\u20131513. https:\/\/doi.org\/10.1002\/ijc.32486 (2020).","journal-title":"Int. J. Cancer"},{"key":"73542_CR7","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1164\/rccm.201505-0990OC","volume":"192","author":"MK Gould","year":"2015","unstructured":"Gould, M. K. et al. Recent trends in the identification of Incidental Pulmonary nodules. Am. J. Respir Crit. Care Med.192, 1208\u20131214. https:\/\/doi.org\/10.1164\/rccm.201505-0990OC (2015).","journal-title":"Am. J. Respir Crit. Care Med."},{"key":"73542_CR8","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1001\/jamainternmed.2018.6277","volume":"179","author":"J Huo","year":"2019","unstructured":"Huo, J., Xu, Y., Sheu, T., Volk, R. J. & Shih, Y. T. Complication rates and downstream medical costs Associated with Invasive Diagnostic procedures for Lung abnormalities in the community setting. JAMA Intern. Med.179, 324\u2013332. https:\/\/doi.org\/10.1001\/jamainternmed.2018.6277 (2019).","journal-title":"JAMA Intern. Med."},{"key":"73542_CR9","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1370\/afm.2519","volume":"18","author":"JR Handy Jr","year":"2020","unstructured":"Handy, J. R. Jr. et al. Results of lung cancer screening in the community. Ann. Fam Med.18, 243\u2013249. https:\/\/doi.org\/10.1370\/afm.2519 (2020).","journal-title":"Ann. Fam Med."},{"key":"73542_CR10","doi-asserted-by":"publisher","first-page":"117727191775160","DOI":"10.1177\/1177271917751608","volume":"13","author":"PJ Mazzone","year":"2018","unstructured":"Mazzone, P. J. et al. Evaluation of a serum lung cancer biomarker panel. Biomark. Insights. 13, 1177271917751608. https:\/\/doi.org\/10.1177\/1177271917751608 (2018).","journal-title":"Biomark. Insights"},{"key":"73542_CR11","doi-asserted-by":"publisher","first-page":"1003","DOI":"10.1016\/j.diii.2016.06.020","volume":"97","author":"D Groheux","year":"2016","unstructured":"Groheux, D. et al. FDG PET-CT for solitary pulmonary nodule and lung cancer: Literature review. Diagn. Interv Imaging. 97, 1003\u20131017. https:\/\/doi.org\/10.1016\/j.diii.2016.06.020 (2016).","journal-title":"Diagn. Interv Imaging"},{"key":"73542_CR12","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1186\/s12943-022-01505-z","volume":"21","author":"W Li","year":"2022","unstructured":"Li, W. et al. Liquid biopsy in lung cancer: Significance in diagnostics, prediction, and treatment monitoring. Mol. Cancer. 21, 25. https:\/\/doi.org\/10.1186\/s12943-022-01505-z (2022).","journal-title":"Mol. Cancer"},{"key":"73542_CR13","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1186\/s13045-022-01351-y","volume":"15","author":"M Nikanjam","year":"2022","unstructured":"Nikanjam, M., Kato, S. & Kurzrock, R. Liquid biopsy: Current technology and clinical applications. J. Hematol. Oncol.15, 131. https:\/\/doi.org\/10.1186\/s13045-022-01351-y (2022).","journal-title":"J. Hematol. Oncol."},{"key":"73542_CR14","doi-asserted-by":"publisher","unstructured":"Schochter, F. et al. Are circulating Tumor cells (CTCs) ready for clinical use in breast Cancer? An overview of completed and ongoing trials using CTCs for clinical treatment decisions. Cells. 8https:\/\/doi.org\/10.3390\/cells8111412 (2019).","DOI":"10.3390\/cells8111412"},{"key":"73542_CR15","doi-asserted-by":"publisher","first-page":"1559","DOI":"10.1126\/science.1203543","volume":"331","author":"CL Chaffer","year":"2011","unstructured":"Chaffer, C. L. & Weinberg, R. A. A perspective on cancer cell metastasis. Science. 331, 1559\u20131564. https:\/\/doi.org\/10.1126\/science.1203543 (2011).","journal-title":"Science"},{"key":"73542_CR16","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1186\/s12885-022-09472-w","volume":"22","author":"H Yang","year":"2022","unstructured":"Yang, H. et al. Diagnostic value of circulating genetically abnormal cells to support computed tomography for benign and malignant pulmonary nodules. BMC Cancer. 22, 382. https:\/\/doi.org\/10.1186\/s12885-022-09472-w (2022).","journal-title":"BMC Cancer"},{"key":"73542_CR17","doi-asserted-by":"publisher","first-page":"3976","DOI":"10.1158\/1078-0432.CCR-09-3358","volume":"16","author":"RL Katz","year":"2010","unstructured":"Katz, R. L. et al. Genetically abnormal circulating cells in lung cancer patients: An antigen-independent fluorescence in situ hybridization-based case-control study. Clin. Cancer Res.16, 3976\u20133987. https:\/\/doi.org\/10.1158\/1078-0432.CCR-09-3358 (2010).","journal-title":"Clin. Cancer Res."},{"key":"73542_CR18","doi-asserted-by":"publisher","first-page":"3234","DOI":"10.1111\/1759-7714.13654","volume":"11","author":"WR Liu","year":"2020","unstructured":"Liu, W. R. et al. Detection of circulating genetically abnormal cells in peripheral blood for early diagnosis of non-small cell lung cancer. Thorac. Cancer. 11, 3234\u20133242. https:\/\/doi.org\/10.1111\/1759-7714.13654 (2020).","journal-title":"Thorac. Cancer"},{"key":"73542_CR19","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1186\/s12890-023-02433-4","volume":"23","author":"S Tahvilian","year":"2023","unstructured":"Tahvilian, S. et al. The presence of circulating genetically abnormal cells in blood predicts risk of lung cancer in individuals with indeterminate pulmonary nodules. BMC Pulm Med.23, 193. https:\/\/doi.org\/10.1186\/s12890-023-02433-4 (2023).","journal-title":"BMC Pulm Med."},{"key":"73542_CR20","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1007\/s00432-021-03648-w","volume":"148","author":"X Qiu","year":"2022","unstructured":"Qiu, X. et al. Application of circulating genetically abnormal cells in the diagnosis of early-stage lung cancer. J. Cancer Res. Clin. Oncol.148, 685\u2013695. https:\/\/doi.org\/10.1007\/s00432-021-03648-w (2022).","journal-title":"J. Cancer Res. Clin. Oncol."},{"key":"73542_CR21","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1056\/NEJMoa1102873","volume":"365","author":"National Lung Screening Trial Research","year":"2011","unstructured":"National Lung Screening Trial Research. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl. J. Med.365, 395\u2013409. https:\/\/doi.org\/10.1056\/NEJMoa1102873 (2011).","journal-title":"N Engl. J. Med."},{"key":"73542_CR22","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1056\/NEJMoa1911793","volume":"382","author":"HJ de Koning","year":"2020","unstructured":"de Koning, H. J. et al. Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl. J. Med.382, 503\u2013513. https:\/\/doi.org\/10.1056\/NEJMoa1911793 (2020).","journal-title":"N Engl. J. Med."},{"key":"73542_CR23","doi-asserted-by":"publisher","first-page":"e223308","DOI":"10.1148\/radiol.223308","volume":"308","author":"KV Venkadesh","year":"2023","unstructured":"Venkadesh, K. V. et al. Prior CT improves deep learning for malignancy risk estimation of screening-detected pulmonary nodules. Radiology. 308, e223308. https:\/\/doi.org\/10.1148\/radiol.223308 (2023).","journal-title":"Radiology"},{"key":"73542_CR24","doi-asserted-by":"publisher","first-page":"2397","DOI":"10.1007\/s00432-021-03517-6","volume":"147","author":"M Feng","year":"2021","unstructured":"Feng, M. et al. Detection of circulating genetically abnormal cells using 4-color fluorescence in situ hybridization for the early detection of lung cancer. J. Cancer Res. Clin. Oncol.147, 2397\u20132405. https:\/\/doi.org\/10.1007\/s00432-021-03517-6 (2021).","journal-title":"J. Cancer Res. Clin. Oncol."},{"key":"73542_CR25","doi-asserted-by":"publisher","first-page":"e369S","DOI":"10.1378\/chest.12-2362","volume":"143","author":"BD Kozower","year":"2013","unstructured":"Kozower, B. D., Larner, J. M., Detterbeck, F. C. & Jones, D. R. Special treatment issues in non-small cell lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 143, e369S\u2013e399S. https:\/\/doi.org\/10.1378\/chest.12-2362 (2013).","journal-title":"Chest"},{"key":"73542_CR26","doi-asserted-by":"publisher","first-page":"716","DOI":"10.3760\/cma.j.cn112147-20231109-00300","volume":"47","author":"CMA Chinese Thoracic Society","year":"2024","unstructured":"Chinese Thoracic Society, C. M. A. Chinese Alliance against Lung Cancer Expert, G. [Chinese expert consensus on diagnosis and treatment of pulmonary nodules(2024)]. Zhonghua Jie He He Hu Xi Za Zhi. 47, 716\u2013729. https:\/\/doi.org\/10.3760\/cma.j.cn112147-20231109-00300 (2024).","journal-title":"Zhonghua Jie He He Hu Xi Za Zhi"},{"key":"73542_CR27","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1148\/radiol.2017161659","volume":"284","author":"H MacMahon","year":"2017","unstructured":"MacMahon, H. et al. Guidelines for management of Incidental Pulmonary nodules detected on CT images: From the Fleischner Society 2017. Radiology. 284, 228\u2013243. https:\/\/doi.org\/10.1148\/radiol.2017161659 (2017).","journal-title":"Radiology"},{"key":"73542_CR28","doi-asserted-by":"publisher","first-page":"638223","DOI":"10.3389\/fonc.2021.638223","volume":"11","author":"M Ye","year":"2021","unstructured":"Ye, M. et al. Circulating genetically abnormal cells add non-invasive diagnosis value to Discriminate Lung Cancer in patients with Pulmonary nodules \u226410 mm. Front. Oncol.11, 638223. https:\/\/doi.org\/10.3389\/fonc.2021.638223 (2021).","journal-title":"Front. Oncol."},{"key":"73542_CR29","doi-asserted-by":"publisher","first-page":"872","DOI":"10.3978\/j.issn.2072-1439.2014.07.26","volume":"6","author":"YX Wang","year":"2014","unstructured":"Wang, Y. X., Gong, J. S., Suzuki, K. & Morcos, S. K. Evidence based imaging strategies for solitary pulmonary nodule. J. Thorac. Dis.6, 872\u2013887. https:\/\/doi.org\/10.3978\/j.issn.2072-1439.2014.07.26 (2014).","journal-title":"J. Thorac. Dis."},{"key":"73542_CR30","doi-asserted-by":"publisher","first-page":"2680","DOI":"10.1007\/s00330-019-06597-8","volume":"30","author":"G Wu","year":"2020","unstructured":"Wu, G. et al. Preoperative CT-based radiomics combined with intraoperative frozen section is predictive of invasive adenocarcinoma in pulmonary nodules: A multicenter study. Eur. Radiol.30, 2680\u20132691. https:\/\/doi.org\/10.1007\/s00330-019-06597-8 (2020).","journal-title":"Eur. Radiol."},{"key":"73542_CR31","doi-asserted-by":"publisher","first-page":"1312","DOI":"10.1016\/j.jtho.2021.04.007","volume":"16","author":"M Yotsukura","year":"2021","unstructured":"Yotsukura, M. et al. Long-term prognosis of patients with resected Adenocarcinoma in situ and minimally invasive adenocarcinoma of the lung. J. Thorac. Oncol.16, 1312\u20131320. https:\/\/doi.org\/10.1016\/j.jtho.2021.04.007 (2021).","journal-title":"J. Thorac. Oncol."},{"key":"73542_CR32","doi-asserted-by":"publisher","unstructured":"Scafoglio, C. R. et al. Sodium-glucose transporter 2 is a diagnostic and therapeutic target for early-stage lung adenocarcinoma. Sci. Transl Med.10https:\/\/doi.org\/10.1126\/scitranslmed.aat5933 (2018).","DOI":"10.1126\/scitranslmed.aat5933"},{"key":"73542_CR33","doi-asserted-by":"publisher","first-page":"484","DOI":"10.21037\/tlcr.2020.03.33","volume":"9","author":"Y Yu","year":"2020","unstructured":"Yu, Y. et al. Determining the invasiveness of pure ground-glass nodules using dual-energy spectral computed tomography. Transl Lung Cancer Res.9, 484\u2013495. https:\/\/doi.org\/10.21037\/tlcr.2020.03.33 (2020).","journal-title":"Transl Lung Cancer Res."},{"key":"73542_CR34","doi-asserted-by":"publisher","first-page":"2683","DOI":"10.2147\/OTT.S99939","volume":"9","author":"S Zhao","year":"2016","unstructured":"Zhao, S. et al. High expression of Y-box-binding protein 1 correlates with poor prognosis and early recurrence in patients with small invasive lung adenocarcinoma. Onco Targets Ther.9, 2683\u20132692. https:\/\/doi.org\/10.2147\/OTT.S99939 (2016).","journal-title":"Onco Targets Ther."},{"key":"73542_CR35","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1097\/JTO.0b013e318206a221","volume":"6","author":"WD Travis","year":"2011","unstructured":"Travis, W. D. et al. International association for the study of lung cancer\/american thoracic society\/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J. Thorac. Oncol.6, 244\u2013285. https:\/\/doi.org\/10.1097\/JTO.0b013e318206a221 (2011).","journal-title":"J. Thorac. Oncol."},{"key":"73542_CR36","doi-asserted-by":"publisher","first-page":"S2611","DOI":"10.21037\/jtd.2018.05.86","volume":"10","author":"M Sanchez","year":"2018","unstructured":"Sanchez, M., Benegas, M. & Vollmer, I. Management of incidental lung nodules\u2009<\u20098\u00a0mm in diameter. J. Thorac. Dis.10, S2611\u2013S2627. https:\/\/doi.org\/10.21037\/jtd.2018.05.86 (2018).","journal-title":"J. Thorac. Dis."},{"key":"73542_CR37","doi-asserted-by":"publisher","first-page":"1136","DOI":"10.1002\/cam4.303","volume":"3","author":"N Willumsen","year":"2014","unstructured":"Willumsen, N. et al. Serum biomarkers reflecting specific tumor tissue remodeling processes are valuable diagnostic tools for lung cancer. Cancer Med.3, 1136\u20131145. https:\/\/doi.org\/10.1002\/cam4.303 (2014).","journal-title":"Cancer Med."},{"key":"73542_CR38","doi-asserted-by":"publisher","first-page":"190","DOI":"10.3390\/cancers2010190","volume":"2","author":"A Mishra","year":"2010","unstructured":"Mishra, A. & Verma, M. Cancer biomarkers: Are we ready for the prime time? Cancers (Basel). 2, 190\u2013208. https:\/\/doi.org\/10.3390\/cancers2010190 (2010).","journal-title":"Cancers (Basel)"},{"key":"73542_CR39","doi-asserted-by":"publisher","first-page":"1206","DOI":"10.1016\/S1470-2045(23)00444-8","volume":"24","author":"Y Zhang","year":"2023","unstructured":"Zhang, Y. et al. Global variations in lung cancer incidence by histological subtype in 2020: A population-based study. Lancet Oncol.24, 1206\u20131218. https:\/\/doi.org\/10.1016\/S1470-2045(23)00444-8 (2023).","journal-title":"Lancet Oncol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73542-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73542-1","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73542-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,28]],"date-time":"2024-09-28T19:03:38Z","timestamp":1727550218000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73542-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,28]]},"references-count":39,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["73542"],"URL":"https:\/\/doi.org\/10.1038\/s41598-024-73542-1","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,28]]},"assertion":[{"value":"2 April 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 September 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 September 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"22532"}}