A gene-based score for the risk stratification of stage IA lung adenocarcinoma.
IA score
IAExpSuv
LUAD
Prognosis
Risk stratification
Stage IA
Journal
Respiratory research
ISSN: 1465-993X
Titre abrégé: Respir Res
Pays: England
ID NLM: 101090633
Informations de publication
Date de publication:
04 Jan 2024
04 Jan 2024
Historique:
received:
25
09
2022
accepted:
20
12
2023
medline:
5
1
2024
pubmed:
5
1
2024
entrez:
4
1
2024
Statut:
epublish
Résumé
We aim to molecularly stratify stage IA lung adenocarcinoma (LUAD) for precision medicine. Twelve multi-institution datasets (837 cases of IA) were used to classify the high- and low-risk types (based on survival status within 5 years), and the biological differences were compared. Then, a gene-based classifying score (IA score) was trained, tested and validated by several machine learning methods. Furthermore, we estimated the significance of the IA score in the prognostic assessment, chemotherapy prediction and risk stratification of stage IA LUAD. We also developed an R package for the clinical application. The SEER database (15708 IA samples) and TCGA Pan-Cancer (1881 stage I samples) database were used to verify clinical significance. Compared with the low-risk group, the high-risk group of stage IA LUAD has obvious enrichment of the malignant pathway and more driver mutations and copy number variations. The effect of the IA score on the classification of high- and low-risk stage IA LUAD was much better than that of classical clinicopathological factors (training set: AUC = 0.9, validation set: AUC = 0.7). The IA score can significantly predict the prognosis of stage IA LUAD and has a prognostic effect for stage I pancancer. The IA score can effectively predict chemotherapy sensitivity and occult metastasis or invasion in stage IA LUAD. The R package IAExpSuv has a good risk probability prediction effect for both groups and single stages of IA LUAD. The IA score can effectively stratify the risk of stage IA LUAD, offering good assistance in precision medicine.
Identifiants
pubmed: 38178073
doi: 10.1186/s12931-023-02647-4
pii: 10.1186/s12931-023-02647-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
18Subventions
Organisme : National Natural Science Foundation of China
ID : 82002421
Informations de copyright
© 2024. The Author(s).
Références
Baldwin DR, Callister ME. The British Thoracic Society guidelines on the investigation and management of pulmonary nodules. Thorax. 2015;70:794–8.
pubmed: 26135833
doi: 10.1136/thoraxjnl-2015-207221
Wang L, Jiang W, Zhan C, Shi Y, Zhang Y, Lin Z, Yuan Y, Wang Q. Lymph node metastasis in clinical stage IA peripheral lung cancer. Lung Cancer. 2015;90:41–6.
pubmed: 26212683
doi: 10.1016/j.lungcan.2015.07.003
Saji H, Okada M, Tsuboi M, Nakajima R, Suzuki K, Aokage K, Aoki T, Okami J, Yoshino I, Ito H, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer (JCOG0802/WJOG4607L): a multicentre, open-label, phase 3, randomised, controlled, non-inferiority trial. Lancet. 2022;399:1607–17.
pubmed: 35461558
doi: 10.1016/S0140-6736(21)02333-3
Wang C, Yang J, Lu M. Micropapillary predominant lung adenocarcinoma in stage IA benefits from adjuvant chemotherapy. Ann Surg Oncol. 2020;27:2051–60.
pubmed: 31848813
doi: 10.1245/s10434-019-08113-0
Hattori A, Suzuki K, Takamochi K, Wakabayashi M, Aokage K, Saji H, Watanabe SI. Prognostic impact of a ground-glass opacity component in clinical stage IA non-small cell lung cancer. J Thorac Cardiovasc Surg. 2021;161:1469–80.
pubmed: 32451073
doi: 10.1016/j.jtcvs.2020.01.107
Suzuki K, Watanabe SI, Wakabayashi M, Saji H, Aokage K, Moriya Y, Yoshino I, Tsuboi M, Nakamura S, Nakamura K, et al. A single-arm study of sublobar resection for ground-glass opacity dominant peripheral lung cancer. J Thorac Cardiovasc Surg. 2022;163:289-301.e282.
pubmed: 33487427
doi: 10.1016/j.jtcvs.2020.09.146
Liu C, Wang LC, Chen HS, Yeh YC, Hsu PK, Huang CS, Hsieh CC, Hsu HS. Outcomes of patients with different lepidic percentage and tumor size of stage I lung adenocarcinoma. Thorac Cancer. 2022;13:2005–13.
pubmed: 35680127
pmcid: 9284188
doi: 10.1111/1759-7714.14477
Tsuchiya T, Akamine S, Muraoka M, Kamohara R, Tsuji K, Urabe S, Honda S, Yamasaki N. Stage IA non-small cell lung cancer: vessel invasion is a poor prognostic factor and a new target of adjuvant chemotherapy. Lung Cancer. 2007;56:341–8.
pubmed: 17350137
doi: 10.1016/j.lungcan.2007.01.019
Hoadley KA, Yau C, Hinoue T, Wolf DM, Lazar AJ, Drill E, Shen R, Taylor AM, Cherniack AD, Thorsson V, et al. Cell-of-origin patterns dominate the molecular classification of 10,000 tumors from 33 types of cancer. Cell. 2018;173:291-304.e296.
pubmed: 29625048
pmcid: 5957518
doi: 10.1016/j.cell.2018.03.022
Wei L, Jin Z, Yang S, Xu Y, Zhu Y, Ji Y. TCGA-assembler 2: software pipeline for retrieval and processing of TCGA/CPTAC data. Bioinformatics. 2018;34:1615–7.
pubmed: 29272348
doi: 10.1093/bioinformatics/btx812
Zhu Y, Qiu P, Ji Y. TCGA-assembler: open-source software for retrieving and processing TCGA data. Nat Methods. 2014;11:599–600.
pubmed: 24874569
pmcid: 4387197
doi: 10.1038/nmeth.2956
Liu J, Lichtenberg T, Hoadley KA, Poisson LM, Lazar AJ, Cherniack AD, Kovatich AJ, Benz CC, Levine DA, Lee AV, et al. An integrated TCGA pan-cancer clinical data resource to drive high-quality survival outcome analytics. Cell. 2018;173:400-416.e411.
pubmed: 29625055
pmcid: 6066282
doi: 10.1016/j.cell.2018.02.052
Davis S, Meltzer PS. GEOquery: a bridge between the Gene Expression Omnibus (GEO) and BioConductor. Bioinformatics. 2007;23:1846–7.
pubmed: 17496320
doi: 10.1093/bioinformatics/btm254
Doll KM, Rademaker A, Sosa JA. Practical guide to surgical data sets: surveillance, epidemiology, and end results (SEER) database. JAMA Surg. 2018;153:588–9.
pubmed: 29617544
doi: 10.1001/jamasurg.2018.0501
Postmus PE, Kerr KM, Oudkerk M, Senan S, Waller DA, Vansteenkiste J, Escriu C, Peters S. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28:iv1–21.
pubmed: 28881918
doi: 10.1093/annonc/mdx222
Watanabe K, Tsuboi M, Sakamaki K, Nishii T, Yamamoto T, Nagashima T, Ando K, Ishikawa Y, Woo T, Adachi H, et al. Postoperative follow-up strategy based on recurrence dynamics for non-small-cell lung cancer. Eur J Cardiothorac Surg. 2016;49:1624–31.
pubmed: 26792922
doi: 10.1093/ejcts/ezv462
Demicheli R, Fornili M, Ambrogi F, Higgins K, Boyd JA, Biganzoli E, Kelsey CR. Recurrence dynamics for non-small-cell lung cancer: effect of surgery on the development of metastases. J Thorac Oncol. 2012;7:723–30.
pubmed: 22425921
doi: 10.1097/JTO.0b013e31824a9022
Luo J, Schumacher M, Scherer A, Sanoudou D, Megherbi D, Davison T, Shi T, Tong W, Shi L, Hong H, et al. A comparison of batch effect removal methods for enhancement of prediction performance using MAQC-II microarray gene expression data. Pharmacogenomics J. 2010;10:278–91.
pubmed: 20676067
pmcid: 2920074
doi: 10.1038/tpj.2010.57
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43: e47.
pubmed: 25605792
pmcid: 4402510
doi: 10.1093/nar/gkv007
Diaz-Papkovich A, Anderson-Trocmé L, Gravel S. A review of UMAP in population genetics. J Hum Genet. 2021;66:85–91.
pubmed: 33057159
doi: 10.1038/s10038-020-00851-4
Dadu A, Satone VK, Kaur R, Koretsky MJ, Iwaki H, Qi YA, Ramos DM, Avants B, Hesterman J, Gunn R, et al. Application of Aligned-UMAP to longitudinal biomedical studies. Patterns (N Y). 2023;4: 100741.
pubmed: 37409055
doi: 10.1016/j.patter.2023.100741
Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16:284–7.
pubmed: 22455463
pmcid: 3339379
doi: 10.1089/omi.2011.0118
Mayakonda A, Lin DC, Assenov Y, Plass C, Koeffler HP. Maftools: efficient and comprehensive analysis of somatic variants in cancer. Genome Res. 2018;28:1747–56.
pubmed: 30341162
pmcid: 6211645
doi: 10.1101/gr.239244.118
Deo RC. Machine learning in medicine. Circulation. 2015;132:1920–30.
pubmed: 26572668
pmcid: 5831252
doi: 10.1161/CIRCULATIONAHA.115.001593
Greener JG, Kandathil SM, Moffat L, Jones DT. A guide to machine learning for biologists. Nat Rev Mol Cell Biol. 2022;23:40–55.
pubmed: 34518686
doi: 10.1038/s41580-021-00407-0
Tibshirani R. Regression shrinkage and selection via the lasso: a retrospective. J R Stat Soc Ser B Stat Methodol. 2011;73:273–82.
doi: 10.1111/j.1467-9868.2011.00771.x
Lamb J. The Connectivity Map: a new tool for biomedical research. Nat Rev Cancer. 2007;7:54–60.
pubmed: 17186018
doi: 10.1038/nrc2044
Subramanian A, Narayan R, Corsello SM, Peck DD, Natoli TE, Lu X, Gould J, Davis JF, Tubelli AA, Asiedu JK, et al. A next generation connectivity map: L1000 platform and the first 1,000,000 profiles. Cell. 2017;171:1437-1452.e1417.
pubmed: 29195078
pmcid: 5990023
doi: 10.1016/j.cell.2017.10.049
Vickers AJ, Elkin EB. Decision curve analysis: a novel method for evaluating prediction models. Med Decis Making. 2006;26:565–74.
pubmed: 17099194
pmcid: 2577036
doi: 10.1177/0272989X06295361
Chan BKC. Data analysis using R programming. Adv Exp Med Biol. 2018;1082:47–122.
pubmed: 30357717
doi: 10.1007/978-3-319-93791-5_2
Lin S, Lin Y, Nery JR, Urich MA, Breschi A, Davis CA, Dobin A, Zaleski C, Beer MA, Chapman WC, et al. Comparison of the transcriptional landscapes between human and mouse tissues. Proc Natl Acad Sci U S A. 2014;111:17224–9.
pubmed: 25413365
pmcid: 4260565
doi: 10.1073/pnas.1413624111
Ettinger DS, Wood DE, Aisner DL, Akerley W, Bauman JR, Bharat A, Bruno DS, Chang JY, Chirieac LR, D’Amico TA, et al. NCCN guidelines insights: non-small cell lung cancer, version 2.2021. J Natl Compr Canc Netw. 2021;19:254–66.
pubmed: 33668021
doi: 10.6004/jnccn.2021.0013
Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg. 1995;60:615–22 (discussion 622-613).
pubmed: 7677489
doi: 10.1016/0003-4975(95)00537-U
Veluswamy RR, Ezer N, Mhango G, Goodman E, Bonomi M, Neugut AI, Swanson S, Powell CA, Beasley MB, Wisnivesky JP. Limited resection versus lobectomy for older patients with early-stage lung cancer: impact of histology. J Clin Oncol. 2015;33:3447–53.
pubmed: 26240229
pmcid: 4606062
doi: 10.1200/JCO.2014.60.6624
Pignon JP, Tribodet H, Scagliotti GV, Douillard JY, Shepherd FA, Stephens RJ, Dunant A, Torri V, Rosell R, Seymour L, et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol. 2008;26:3552–9.
pubmed: 18506026
doi: 10.1200/JCO.2007.13.9030
Kato H, Ichinose Y, Ohta M, Hata E, Tsubota N, Tada H, Watanabe Y, Wada H, Tsuboi M, Hamajima N, Ohta M. A randomized trial of adjuvant chemotherapy with uracil-tegafur for adenocarcinoma of the lung. N Engl J Med. 2004;350:1713–21.
pubmed: 15102997
doi: 10.1056/NEJMoa032792
Ost D, Goldberg J, Rolnitzky L, Rom WN. Survival after surgery in stage IA and IB non-small cell lung cancer. Am J Respir Crit Care Med. 2008;177:516–23.
pubmed: 18006887
doi: 10.1164/rccm.200706-815OC
Chen D, Wang X, Zhang F, Han R, Ding Q, Xu X, Shu J, Ye F, Shi L, Mao Y, et al. Could tumor spread through air spaces benefit from adjuvant chemotherapy in stage I lung adenocarcinoma? A multi-institutional study. Ther Adv Med Oncol. 2020;12:1758835920978147.
pubmed: 33403018
pmcid: 7739212
doi: 10.1177/1758835920978147
Nicholson AG, Tsao MS, Beasley MB, Borczuk AC, Brambilla E, Cooper WA, Dacic S, Jain D, Kerr KM, Lantuejoul S, et al. The 2021 WHO classification of lung tumors: impact of advances since 2015. J Thorac Oncol. 2021;17:362–87.
pubmed: 34808341
doi: 10.1016/j.jtho.2021.11.003
Travis WD, Asamura H, Bankier AA, Beasley MB, Detterbeck F, Flieder DB, Goo JM, MacMahon H, Naidich D, Nicholson AG, et al. The IASLC Lung Cancer Staging Project: proposals for coding T categories for subsolid nodules and assessment of tumor size in part-solid tumors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol. 2016;11:1204–23.
pubmed: 27107787
doi: 10.1016/j.jtho.2016.03.025
Hattori A, Matsunaga T, Takamochi K, Oh S, Suzuki K. Neither maximum tumor size nor solid component size is prognostic in part-solid lung cancer: impact of tumor size should be applied exclusively to solid lung cancer. Ann Thorac Surg. 2016;102:407–15.
pubmed: 27177840
doi: 10.1016/j.athoracsur.2016.02.074
Ye T, Deng L, Wang S, Xiang J, Zhang Y, Hu H, Sun Y, Li Y, Shen L, Xie L, et al. Lung adenocarcinomas manifesting as radiological part-solid nodules define a special clinical subtype. J Thorac Oncol. 2019;14:617–27.
pubmed: 30659988
doi: 10.1016/j.jtho.2018.12.030
Strauss GM, Herndon JE 2nd, Maddaus MA, Johnstone DW, Johnson EA, Harpole DH, Gillenwater HH, Watson DM, Sugarbaker DJ, Schilsky RL, et al. Adjuvant paclitaxel plus carboplatin compared with observation in stage IB non-small-cell lung cancer: CALGB 9633 with the Cancer and Leukemia Group B, Radiation Therapy Oncology Group, and North Central Cancer Treatment Group Study Groups. J Clin Oncol. 2008;26:5043–51.
pubmed: 18809614
pmcid: 2652093
doi: 10.1200/JCO.2008.16.4855
Butts CA, Ding K, Seymour L, Twumasi-Ankrah P, Graham B, Gandara D, Johnson DH, Kesler KA, Green M, Vincent M, et al. Randomized phase III trial of vinorelbine plus cisplatin compared with observation in completely resected stage IB and II non-small-cell lung cancer: updated survival analysis of JBR-10. J Clin Oncol. 2010;28:29–34.
pubmed: 19933915
doi: 10.1200/JCO.2009.24.0333
Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J. Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N Engl J Med. 2004;350:351–60.
pubmed: 14736927
doi: 10.1056/NEJMoa031644
Winton T, Livingston R, Johnson D, Rigas J, Johnston M, Butts C, Cormier Y, Goss G, Inculet R, Vallieres E, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med. 2005;352:2589–97.
pubmed: 15972865
doi: 10.1056/NEJMoa043623
Douillard JY, Rosell R, De Lena M, Carpagnano F, Ramlau R, Gonzáles-Larriba JL, Grodzki T, Pereira JR, Le Groumellec A, Lorusso V, et al. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol. 2006;7:719–27.
pubmed: 16945766
doi: 10.1016/S1470-2045(06)70804-X
Altorki N, Wang X, Kozono D, Watt C, Landrenau R, Wigle D, Port J, Jones DR, Conti M, Ashrafi AS, et al. Lobar or sublobar resection for peripheral stage IA non-small-cell lung cancer. N Engl J Med. 2023;388:489–98.
pubmed: 36780674
pmcid: 10036605
doi: 10.1056/NEJMoa2212083
Zhu J, Fan Y, Xiong Y, Wang W, Chen J, Xia Y, Lei J, Gong L, Sun S, Jiang T. Delineating the dynamic evolution from preneoplasia to invasive lung adenocarcinoma by integrating single-cell RNA sequencing and spatial transcriptomics. Exp Mol Med. 2022;54:2060–76.
pubmed: 36434043
pmcid: 9722784
doi: 10.1038/s12276-022-00896-9
Chen H, Carrot-Zhang J, Zhao Y, Hu H, Freeman SS, Yu S, Ha G, Taylor AM, Berger AC, Westlake L, et al. Genomic and immune profiling of pre-invasive lung adenocarcinoma. Nat Commun. 2019;10:5472.
pubmed: 31784532
pmcid: 6884501
doi: 10.1038/s41467-019-13460-3
Hu X, Fujimoto J, Ying L, Fukuoka J, Ashizawa K, Sun W, Reuben A, Chow CW, McGranahan N, Chen R, et al. Multi-region exome sequencing reveals genomic evolution from preneoplasia to lung adenocarcinoma. Nat Commun. 2019;10:2978.
pubmed: 31278276
pmcid: 6611767
doi: 10.1038/s41467-019-10877-8
Zhang C, Zhang J, Xu FP, Wang YG, Xie Z, Su J, Dong S, Nie Q, Shao Y, Zhou Q, et al. Genomic landscape and immune microenvironment features of preinvasive and early invasive lung adenocarcinoma. J Thorac Oncol. 2019;14:1912–23.
pubmed: 31446140
pmcid: 6986039
doi: 10.1016/j.jtho.2019.07.031
Wang Z, Li Z, Zhou K, Wang C, Jiang L, Zhang L, Yang Y, Luo W, Qiao W, Wang G, et al. Deciphering cell lineage specification of human lung adenocarcinoma with single-cell RNA sequencing. Nat Commun. 2021;12:6500.
pubmed: 34764257
pmcid: 8586023
doi: 10.1038/s41467-021-26770-2
Xing X, Yang F, Huang Q, Guo H, Li J, Qiu M, Bai F, Wang J. Decoding the multicellular ecosystem of lung adenocarcinoma manifested as pulmonary subsolid nodules by single-cell RNA sequencing. Sci Adv. 2021;7:eabd9738.
pubmed: 33571124
pmcid: 7840134
doi: 10.1126/sciadv.abd9738