A prognostic framework for predicting lung signet ring cell carcinoma via a machine learning based cox proportional hazard model.


Journal

Journal of cancer research and clinical oncology
ISSN: 1432-1335
Titre abrégé: J Cancer Res Clin Oncol
Pays: Germany
ID NLM: 7902060

Informations de publication

Date de publication:
25 Jul 2024
Historique:
received: 05 08 2023
accepted: 08 07 2024
medline: 26 7 2024
pubmed: 26 7 2024
entrez: 25 7 2024
Statut: epublish

Résumé

Signet ring cell carcinoma (SRCC) is a rare type of lung cancer. The conventional survival nomogram used to predict lung cancer performs poorly for SRCC. Therefore, a novel nomogram specifically for studying SRCC is highly required. Baseline characteristics of lung signet ring cell carcinoma were obtained from the Surveillance, Epidemiology, and End Results (SEER) database. Univariate and multivariate Cox regression and random forest analysis were performed on the training group data, respectively. Subsequently, we compared results from these two types of analyses. A nomogram model was developed to predict 1-year, 3-year, and 5-year overall survival (OS) for patients, and receiver operating characteristic (ROC) curves and calibration curves were used to assess the prediction accuracy. Decision curve analysis (DCA) was used to assess the clinical applicability of the proposed model. For treatment modalities, Kaplan-Meier curves were adopted to analyze condition-specific effects. We obtained 731 patients diagnosed with lung signet ring cell carcinoma (LSRCC) in the SEER database and randomized the patients into a training group (551) and a validation group (220) with a ratio of 7:3. Eight factors including age, primary site, T, N, and M.Stage, surgery, chemotherapy, and radiation were included in the nomogram analysis. Results suggested that treatment methods (like surgery, chemotherapy, and radiation) and T-Stage factors had significant prognostic effects. The results of ROC curves, calibration curves, and DCA in the training and validation groups demonstrated that the nomogram we constructed could precisely predict survival and prognosis in LSRCC patients. Through deep verification, we found the constructed model had a high C-index, indicating that the model had a strong predictive power. Further, we found that all surgical interventions had good effects on OS and cancer-specific survival (CSS). The survival curves showed a relatively favorable prognosis for T0 patients overall, regardless of the treatment modality. Our nomogram is demonstrated to be clinically beneficial for the prognosis of LSRCC patients. The surgical intervention was successful regardless of the tumor stage, and the Cox proportional hazard (CPH) model had better performance than the machine learning model in terms of effectiveness.

Identifiants

pubmed: 39052087
doi: 10.1007/s00432-024-05886-0
pii: 10.1007/s00432-024-05886-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

364

Subventions

Organisme : the Science and Technology Special Project of Zhanjiang
ID : (2022A01034)
Organisme : The Guangdong Provincial Department of Education Research Project
ID : (2022KTSCX)

Informations de copyright

© 2024. The Author(s).

Références

Akira Okimura H, Hirano Ylto et al (2023) Primary lung adenocarcinoma with ALK gene rearrangement mostly occupied by the signet-ring cell carcinoma component: a case report. Cureus 15(9):e45068
pubmed: 37842503 pmcid: 10568040
Anwar S, Acharya S, Elsayegh D et al (2020) Life threatening haemoptysis in primary lung cancer-signet ring cell carcinoma. Respir Med Case Rep 31:101195
pubmed: 32913701 pmcid: 7472919
Baralou V, Kalpourtzi N, Touloumi G (2023) Individual risk prediction: comparing random forests with Cox proportional-hazards model by a simulation study. Biom J 65(6):e2100380
doi: 10.1002/bimj.202100380 pubmed: 36169048
Boland JM, Wampfler JA, Jang JS et al (2014) Pulmonary adenocarcinoma with signet ring cell features: a comprehensive study from 3 distinct patient cohorts. Am J Surg Pathol 38(12):1681–1688
doi: 10.1097/PAS.0000000000000280 pubmed: 25007143 pmcid: 4410841
Cai Y, Xie Y, Xiong Y et al (2021) Clinicopathological characteristics and survival in lung signet ring cell carcinoma: a population-based study. Bosn J Basic Med Sci 21(6):752–759
pubmed: 33596400 pmcid: 8554702
Campbell JD, Alexandrov A, Kim J et al (2016) Distinct patterns of somatic genome alterations in lung adenocarcinomas and squamous cell carcinomas. Nat Genet 48(6):607–616
doi: 10.1038/ng.3564 pubmed: 27158780 pmcid: 4884143
Chen C, Wang L, Gu C et al (2020a) Survival analyses and immunohistochemical study of primary signet ring cell carcinoma of the lung adenocarcinoma. Transl Cancer Res 9(2):620–628
doi: 10.21037/tcr.2019.11.54 pubmed: 35117407 pmcid: 8797340
Chen X, Wang X, Chen K et al (2020b) Comparison of survival distributions in clinical trials: a practical guidance. Clin Trials 17(5):507–521
doi: 10.1177/1740774520928614 pubmed: 32594788
Coutant C, Olivier C, Lambaudie E et al (2009) Comparison of models to predict nonsentinel lymph node status in breast cancer patients with metastatic sentinel lymph nodes: a prospective multicenter study. J Clin Oncol 27(17):2800–2808
doi: 10.1200/JCO.2008.19.7418 pubmed: 19349546
Deo RC (2015) Machine learning in Medicine. Circulation 132(20):1920–1930
doi: 10.1161/CIRCULATIONAHA.115.001593 pubmed: 26572668 pmcid: 5831252
Frost AR, Terahata S, Fau - Yeh IT, Yeh It Fau -, Siegel RS et al (1995) The significance of signet ring cells in infiltrating lobular carcinoma of the breast. Arch Pathol Lab Med 119(1):64–68
pubmed: 7802556
Hao Y-Q, Tang H-P, Liu H-Y (2015) Primary signet-ring cell carcinoma of the lung treated with crizotinib: a case report. Oncol Lett 9(5):2205–2207
doi: 10.3892/ol.2015.3003 pubmed: 26137041 pmcid: 4467348
Hayashi H, Kitamura H, Nakatani Y et al (1999) Primary signet-ring cell carcinoma of the lung: histochemical and immunohistochemical characterization. Hum Pathol 30(4):378–383
doi: 10.1016/S0046-8177(99)90111-9 pubmed: 10208457
Iasonos A, Schrag D, Raj GV et al (2008) How to build and interpret a nomogram for cancer prognosis. J Clin Oncol 26(8):1364–1370
doi: 10.1200/JCO.2007.12.9791 pubmed: 18323559
Iwasaki T, Fau - Ohta M, Ohta M, Fau - Lefor AT et al (2008) Signet-ring cell carcinoma component in primary lung adenocarcinoma: potential prognostic factor. Histopathology 52(5):639–640Lefor At Fau - Kawahara K
Kattan MW, Leung Dh Fau -, Brennan MF, Brennan MF (2002) Postoperative nomogram for 12-year sarcoma-specific death. J Clin Oncol 20(3):791–796
doi: 10.1200/JCO.2002.20.3.791 pubmed: 11821462
Kitamura H, Fau - Sumikawa T, Sumikawa T, Fau - Fukuoka H, Fukuoka H, Fau - Kanisawa M et al (1985) Primary signet-ring cell carcinoma of the urinary bladder. Report of two cases with histochemical studies. Acta Pathol Jpn 35(3):675–686
pubmed: 2994357
Kwak EL, Bang YJ, Camidge DR et al (2010) Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 363:1693–1703
doi: 10.1056/NEJMoa1006448 pubmed: 20979469 pmcid: 3014291
lbrahim Yildiz (2021) Liver and pancreatic Injury in response to ALK inhibitors in a patient with primary Signet Ring Cell Carcinoma of the lung: a Case Report. Case Rep Oncol 14(1):107–111
doi: 10.1159/000512829
Liang W, Zhang L, Jiang G et al (2015) Development and validation of a nomogram for predicting survival in patients with resected non-small-cell lung cancer. J Clin Oncol 33(8):861–869
doi: 10.1200/JCO.2014.56.6661 pubmed: 25624438
Liu FX, Dai YR (2022) Product Processing Quality Classification Model for Small-Sample and Imbalanced Data Environment. Comput Intell Neurosci 2022: 9024165
Liu Z, Jiang Z, Meng L et al (2021) Handcrafted and Deep Learning-Based Radiomic Models Can Distinguish GBM from Brain Metastasis. J Oncol 2021:5518717
Livieratos S, Smith JK, Fatakhov E et al (2013) Primary signet ring cell carcinoma of the lung: a rare subtype. BMJ case Rep 2013:bcr2013200111
doi: 10.1136/bcr-2013-200111 pubmed: 24057330 pmcid: 3794152
Ma YR, Ren Z, Conner MG et al (2017) Reduced E-Cadherin and aberrant β-Catenin expression are Associated with Advanced Disease in Signet-Ring Cell Carcinomas. Appl Immunohistochem Mol Morphol 25(6):432–438
doi: 10.1097/PAI.0000000000000317 pubmed: 26808130
Mogensen UB, Ishwaran H, Gerds TA (2012) Evaluating Random Forests for Survival Analysis using Prediction Error curves. J Stat Softw 50(11):1–23
doi: 10.18637/jss.v050.i11 pubmed: 25317082 pmcid: 4194196
Moolgavkar SH, Chang ET, Watson HN et al (2018) An Assessment of the Cox proportional hazards regression model for epidemiologic studies. Risk Anal 38(4):777–794
doi: 10.1111/risa.12865 pubmed: 29168991
Moon KC, Cho SY, Lee HS et al (2006) Distinct expression patterns of E-cadherin and beta-catenin in signet ring cell carcinoma components of primary pulmonary adenocarcinoma. Arch Pathol Lab Med 130(9):1320–1325
doi: 10.5858/2006-130-1320-DEPOEA pubmed: 16948518
Moran CA (2006) Pulmonary adenocarcinoma: the expanding spectrum of histologic variants. Arch Pathol Lab Med 130(7):958–962
doi: 10.5858/2006-130-958-PATESO pubmed: 16831050
Niu Z, Jin R, Zhang Y et al (2022) Signaling pathways and targeted therapies in lung squamous cell carcinoma: mechanisms and clinical trials. Signal Transduct Target Ther 7(1):353
doi: 10.1038/s41392-022-01200-x pubmed: 36198685 pmcid: 9535022
Park SH, Goo JM, Jo C-H (2004) Receiver operating characteristic (ROC) curve: practical review for radiologists. Korean J Radiol 5(1):11–18
doi: 10.3348/kjr.2004.5.1.11 pubmed: 15064554 pmcid: 2698108
Poon V, Lu D (2022) Performance of Cox proportional hazard models on recovering the ground truth of confounded exposure-response relationships for large-molecule oncology drugs. CPT Pharmacometrics Syst Pharmacol 11(11):1511–1526
doi: 10.1002/psp4.12859 pubmed: 35988264 pmcid: 9662202
Qiu X, Gao J, Yang J et al (2020) A Comparison Study of Machine Learning (Random Survival Forest) and Classic Statistic (Cox Proportional Hazards) for Predicting Progression in High-Grade Glioma after Proton and Carbon Ion Radiotherapy. Front Oncol 10:551420
doi: 10.3389/fonc.2020.551420 pubmed: 33194609 pmcid: 7662123
Randolph TL, Amin Mb Fau - Ro JY, Ro Jy Fau -, Ayala AG et al (1997) Histologic variants of adenocarcinoma and other carcinomas of prostate: pathologic criteria and clinical significance. Mod Pathol 10(6):612 – 29
Sung H, Ferlay J, Siegel RL et al (2021) Global Cancer statistics 2020: GLOBOCAN estimates of incidence and Mortality Worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249
doi: 10.3322/caac.21660 pubmed: 33538338
Testori A, Perroni G, Carlo C et al (2021) Primary signet-ring cell carcinoma of the lung in an HIV-positive patient. Thorac Cancer 12(7):1122–1125
doi: 10.1111/1759-7714.13887 pubmed: 33594833 pmcid: 8017251
Wang H, Li G (2017) A selective review on Random Survival forests for high Dimensional Data. Quant Biosci 36(2):85–96
pubmed: 30740388 pmcid: 6364686
Wang Y, Wang Y, Li J et al (2020) Primary signet-ring cell carcinoma of the lung: a report of seven cases. Thorac Cancer 11(10):3015–3019
doi: 10.1111/1759-7714.13614 pubmed: 32812677 pmcid: 7529556
Wang Y, Deng Y, Tan Y et al (2023) A comparison of random survival forest and Cox regression for prediction of mortality in patients with hemorrhagic stroke. BMC Med Inf Decis Mak 23(1):215
doi: 10.1186/s12911-023-02293-2
Wu SG, Chen XT, Zhang WW et al (2018) Survival in signet ring cell carcinoma varies based on primary tumor location: a Surveillance, Epidemiology, and end results database analysis. Expert Rev Gastroenterol Hepatol 12(2):209–214
doi: 10.1080/17474124.2018.1416291 pubmed: 29227748
Yamashina M (1986) A variant of early gastric carcinoma. Histologic and histochemical studies of early signet ring cell carcinomas discovered beneath preserved surface epithelium. Cancer 15(6):1333–1339
doi: 10.1002/1097-0142(19860915)58:6<1333::AID-CNCR2820580625>3.0.CO;2-B
Yiğit N, Çelik E, Fau - Yavan İ, Yavan İ (2018) Prominent Signet Ring Cell morphology in a pulmonary squamous cell carcinoma. Turk Patoloji Derg 34(2):194–197
pubmed: 28272660
Zhang H, Naji Y, Yan M et al (2020) Development and validation of prognostic nomograms in patients with adrenocortical carcinoma: a population-based study. Int Urol Nephrol 52(6):1057–1071
doi: 10.1007/s11255-020-02413-1 pubmed: 32072388
Zheng XQ, Huang JF, Lin JL et al (2019) Incidence, prognostic factors, and a nomogram of lung cancer with bone metastasis at initial diagnosis: a population-based study. Transl Lung Cancer Res 8(4):367–379
doi: 10.21037/tlcr.2019.08.16 pubmed: 31555512 pmcid: 6749127

Auteurs

Haixin Chen (H)

The First Clinical College, Guangdong Medical University, Zhanjiang, Guangdong, 524023, China.

Yanyan Xu (Y)

The First Clinical College, Guangdong Medical University, Zhanjiang, Guangdong, 524023, China.

Haowen Lin (H)

The First Clinical College, Guangdong Medical University, Zhanjiang, Guangdong, 524023, China.

Shibiao Wan (S)

Department of Genetics, Cell Biology and Anatomy, University of Nebraska Medical Center, Omaha, NE, USA. swan@unmc.edu.

Lianxiang Luo (L)

The Marine Biomedical Research Institute of Guangdong Zhanjiang, School of Ocean and Tropical Medicine, Guangdong Medical University, Zhanjiang, Guangdong, 524023, China. luolianxiang321@gdmu.edu.cn.

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