ArticleJournal of clinical oncology : official journal of the American Society of Clinical Oncology2015
Subtype Classification of Lung Adenocarcinoma Predicts Benefit From Adjuvant Chemotherapy in Patients Undergoing Complete Resection.
Registry-linked trialAbstract read
In one paragraph
Article in Journal of clinical oncology : official journal of the American Society of Clinical Oncology, 2015. The graph could read no effect estimate from its abstract, so it casts no vote on the map. It is linked to trial NCT03380468 (Adjuvant Chemotherapy Versus Observation in Fully Resected Stage I Lung Adenocarcinoma With High Risk of Post-operative Recurrence), which is not on this map. Cited by 150 papers, 1 of them a synthesis that pooled it.
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150citing papers in PubMed, 1 pooled it
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What it found
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The trial behind it
Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.
NCT03380468 phase2 / phase3unknown statusnot on this mapstarted 2018, after this paper: background citation
Adjuvant Chemotherapy Versus Observation in Fully Resected Stage I Lung Adenocarcinoma With High Risk of Post-operative Recurrence
Who cites it
150 citing papers in PubMed, 1 synthesis or guideline pooled it.
- Efficacy and Benefit of Postoperative Chemotherapy in Micropapillray or Solid Predominant Pattern in Stage IB Lung Adenocarcinoma: A Systematic Review and Meta-Analysis.Frontiers in surgery · 2021Pooled it
- Early2 factor (E2F) deregulation is a prognostic and predictive biomarker in lung adenocarcinoma.Oncotarget · 2016Trial
- Integration of Histologic Pattern Classifiers and Graph Convolutional Networks for Prognostic Prediction in Lung Adenocarcinoma.JTO clinical and research reports · 2026Article
- Topologically distinct intratumoral heterogeneity scores for predicting high-risk pathological grades in invasive lung adenocarcinoma: A multicenter study across four institutions.PLOS digital health · 2026Article
- Biopsies Can Predict Lung Adenocarcinoma IASLC Grade: A New Proposal and Grading Pitfalls.JTO clinical and research reports · 2026Article
- Does lung adenocarcinoma subtyping offer clinical benefits?-a retrospective population-based cohort study from Sweden.Annals of translational medicine · 2026Article
- Application of SHAP visualization and nomogram based on PET/CT radiomics combined models for risk stratification in high-grade invasive lung adenocarcinoma.Journal of translational medicine · 2026Article
- The IASLC grading system as a predictor for EGFR-TKI therapy in patients withTranslational lung cancer research · 2026Article
- Radiological, Molecular, and Pathological Factors Unite: A Model for Predicting Recurrence-Free Survival in Pathological Stage I Lung Adenocarcinoma.Thoracic cancer · 2026Article
- European prognosis evaluation of early-stage lung adenocarcinoma patterns after lobectomy versus segmentectomy based on clinical stage settings.JTCVS open · 2026Article
- The impact of predominant histopathological pattern and other histopathological factors on survival in pulmonary adenocarcinomas.Turk gogus kalp damar cerrahisi dergisi · 2026Article
- Deciphering the intratumoral histologic heterogeneity of lung adenocarcinoma using radiomics.European radiology · 2025Article
- Enhancing the intraoperative identification of high-grade patterns in invasive lung adenocarcinoma via radiomics.Translational lung cancer research · 2025Article
- Adjuvant pembrolizumab therapy for completely resected stage I lung adenocarcinoma with micropapillary or solid histological subtypes: a single-center, single-arm, phase 2 trial.EClinicalMedicine · 2025Article
- Excessive MYC Orchestrates Macrophages induced Chromatin Remodeling to Sustain Micropapillary-Patterned Malignancy in Lung Adenocarcinoma.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025Article
- Impact of histopathological subtypes on invasive lung adenocarcinoma: from epidemiology to tumour microenvironment to therapeutic strategies.World journal of surgical oncology · 2025Review
- Predicting malignant risk of ground-glass nodules using convolutional neural networks based on dual-time-pointCancer imaging : the official publication of the International Cancer Imaging Society · 2025Article
- Prognostic value of ground-glass opacity on computed tomography for patients with pathological stage IA3 lung adenocarcinoma: a multicenter retrospective cohort study.Translational lung cancer research · 2024Article
- Prognostic significance using histologic subtype in stage I lung adenocarcinoma.Journal of thoracic disease · 2024Article
- Histopathologic pattern and molecular risk stratification are associated with prognosis in patients with stage IB lung adenocarcinoma.Translational lung cancer research · 2024Article
90 more citing papers are in PubMed but not listed here.
Corrections and comments
PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.
Authors and funding
15 authors.
Ming-Sound TsaoMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain. ming.tsao@uhn.ca.
Sophie MarguetMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Gwénaël Le TeuffMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Sylvie LantuejoulMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Frances A ShepherdMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Lesley SeymourMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Robert KratzkeMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Stephen L GrazianoMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Helmut H PopperMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Rafael RosellMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Jean-Yves DouillardMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Thierry Le-ChevalierMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Jean-Pierre PignonMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Jean-Charles SoriaMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Elisabeth M BrambillaMing-Sound Tsao and Frances A. Shepherd, Princess Margaret Cancer Centre, University Health Network, and University of Toronto, Toronto; Lesley Seymour, NCIC Clinical Trials Group and Queen's University, Kingston, Ontario, Canada; Sophie Marguet, Gwénaël Le Teuff, Thierry Le-Chevalier, Jean-Pierre Pignon, and Jean-Charles Soria, Gustave Roussy, Villejuif; Sylvie Lantuejoul and Elisabeth M. Brambilla, Inserm U823, Centre Hospitalier Universitaire de Grenoble, Institut Albert Bonniot, Université Joseph Fourier, Grenoble; Jean-Yves Douillard, Centre René Gauducheau, Saint-Herblain, Nantes, France; Robert Kratzke, University of Minnesota, Minneapolis, MN; Stephen L. Graziano, SUNY Upstate Medical University, Syracuse, NY; Helmut H. Popper, Institute of Pathology, University Medical School of Graz, Graz, Austria; and Rafael Rosell, Catalan Institute of Oncology, Barcelona, Spain.
Funding
Member Site CoreU10CA180821 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI Evanthia Galanis · 2014 to 2026
$177.3MTHE ALLIANCE NCTN BIOREPOSITORY AND BIOSPECIMEN RESOURCEU24CA196171 · NCI · WASHINGTON UNIVERSITY · PI Mine Cicek, Wendy Frankel · 2015 to 2026
$35.0MLACE-Bio-II: Identification, validation and implementation of prognostic and/or pR01CA165958 · NCI · QUEEN'S UNIVERSITY AT KINGSTON · PI SEYMOUR, LESLEY KATIE · 2012 to 2016
$2.3MNCI NIH HHS R01 CA165958NCI NIH HHS U10 CA180821NCI NIH HHS U24 CA196171
Abstract
purposeThe classification for invasive lung adenocarcinoma by the International Association for the Study of Lung Cancer, American Thoracic Society, European Respiratory Society, and WHO is based on the predominant histologic pattern-lepidic (LEP), papillary (PAP), acinar (ACN), micropapillary (MIP), or solid (SOL)-present in the tumor. This classification has not been tested in multi-institutional cohorts or clinical trials or tested for its predictive value regarding survival from adjuvant chemotherapy (ACT). PATIENTS AND
methodsOf 1,766 patients in the IALT, JBR.10, CALGB 9633 (Alliance), and ANITA ACT trials included in the LACE-Bio study, 725 had adenocarcinoma. Histologies were reclassified according to the new classification and then collapsed into three groups (LEP, ACN/PAP, and MIP/SOL). Primary end point was overall survival (OS); secondary end points were disease-free survival (DFS) and specific DFS (SDFS). Hazard ratios (HRs) and 95% CIs were estimated through multivariable Cox models stratified by trial. Prognostic value was estimated in the observation arm and predictive value by a treatment effect interaction with histologic subgroups. Significance level was set at .01 for pooled analysis.
resultsA total of 575 patients were included in this analysis. OS was not prognostically different between histologic subgroups, but univariable DFS and SDFS were worse for MIP/SOL compared with LEP or ACN/PAP subgroup (P < .01); this remained marginally significant after adjustment. MIP/SOL patients (but not ACN/PAP) derived DFS and SDFS but not OS benefit from ACT (OS: HR, 0.71; 95% CI, 0.51 to 0.99; interaction P = .18; DFS: HR, 0.60; 95% CI, 0.44 to 0.82; interaction P = < .01; and SDFS: HR, 0.59; 95% CI, 0.42 to 0.81; interaction P = .01).
conclusionThe new lung adenocarcinoma classification based on predominant histologic pattern was not predictive for ACT benefit for OS, but it seems predictive for disease-specific outcomes.
Indexed as
AdenocarcinomaAdenocarcinoma of LungAgedChemotherapy, AdjuvantFemaleHumansLung NeoplasmsMaleMiddle AgedPredictive Value of TestsPrognosisSurvival Rate
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NCT03380468ClinicalTrials.gov
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