ArticleCarcinogenesis2018
Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population.
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Article in Carcinogenesis, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 26 papers, 6 of them syntheses that pooled it.
0numbers the graph read from it
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26citing papers in PubMed, 6 pooled it
2.4field-weighted citation impact, top 11% of its field
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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.
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Who cites it
26 citing papers in PubMed, 6 syntheses or guidelines pooled it, 37 citations in OpenAlex.
- Genome-wide association study of lung adenocarcinoma in East Asia and comparison with a European population.Nature communications · 2023Pooled it
- A systematic review of genetic ancestry as a risk factor for incidence of non-small cell lung cancer in the US.Frontiers in genetics · 2023Pooled it
- Construction and case study of a novel lung cancer risk index.BMC cancer · 2022Pooled it
- Cross-ancestry genome-wide meta-analysis of 61,047 cases and 947,237 controls identifies new susceptibility loci contributing to lung cancer.Nature genetics · 2022Pooled it
- Impact of Smoking on Response to the First-Line Treatment of Advanced ALK-Positive Non-Small Cell Lung Cancer: A Bayesian Network Meta-Analysis.Frontiers in pharmacology · 2022Pooled it
- Potential genetic modifiers for somatic EGFR mutation in lung cancer: a meta-analysis and literature review.BMC cancer · 2019Pooled it
- Knowledge-Guided Explainable Recommendation Tool for Cancer Risk Prediction Models Using Retrieval-Augmented Large Language Models: Development and Validation Study.JMIR medical informatics · 2026Article
- Crosstalk between metabolic reprogramming and microbiota: implications for cancer progression and novel therapeutic opportunities.Frontiers in immunology · 2025Review
- Single nucleotide variants in lung cancer.Chinese medical journal pulmonary and critical care medicine · 2024Review
- Symbiotic microbial communities in various locations of the lung cancer respiratory tract along with potential host immunological processes affected.Frontiers in cellular and infection microbiology · 2024Review
- Candidate pathway analysis of surfactant proteins identifies CTSH and SFTA2 that influences lung cancer risk.Human molecular genetics · 2023Article
- Genome-wide Interaction Study with Smoking for Colorectal Cancer Risk Identifies Novel Genetic Loci Related to Tumor Suppression, Inflammation, and Immune Response.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2023Article
- The Importance of the Immune System and Molecular Cell Signaling Pathways in the Pathogenesis and Progression of Lung Cancer.International journal of molecular sciences · 2023Review
- Association of psychological distress, smoking and genetic risk with the incidence of lung cancer: a large prospective population-based cohort study.Frontiers in oncology · 2023Article
- Gut microbiota and its metabolites in non-small cell lung cancer and brain metastasis: from alteration to potential microbial markers and drug targets.Frontiers in cellular and infection microbiology · 2023Article
- Genome-wide interaction analysis identified low-frequency variants with sex disparity in lung cancer risk.Human molecular genetics · 2022Article
- Association of smoking and polygenic risk with the incidence of lung cancer: a prospective cohort study.British journal of cancer · 2022Article
- microRNA-1321 and microRNA-7515 contribute to the progression of non-small cell lung cancer by targeting CDC20.The Kaohsiung journal of medical sciences · 2022Article
- Alterations of the Human Lung and Gut Microbiomes in Non-Small Cell Lung Carcinomas and Distant Metastasis.Microbiology spectrum · 2021Article
- Polymorphisms in the Gene Encoding Caspase 8 May Predict the Response to First-Line Platinum-Based Chemotherapy in Locally Advanced or Advanced Non-Small-Cell Lung Cancer.Journal of clinical medicine · 2021Article
Corrections and comments
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Authors and funding
76 authors at 20 institutions in 19 countries.
Yafang LiBiomedical Data Science Department, Dartmouth College, Hanover, NH, USA.
Xiangjun XiaoBiomedical Data Science Department, Dartmouth College, Hanover, NH, USA.
Younghun HanBiomedical Data Science Department, Dartmouth College, Hanover, NH, USA.
Olga GorlovaBiomedical Data Science Department, Dartmouth College, Hanover, NH, USA.
David QianBiomedical Data Science Department, Dartmouth College, Hanover, NH, USA.
Natasha LeighlDepartment of Medicine, The Princess Margaret Cancer Center, University Health Network, Toronto, ON, Canada.
Jakob S JohansenDepartment of Oncology, Herlev and Gentofte Hospital, Copenhagen University Hospital, Copenhagen University, Herlev, Denmark.
Matt BarnettPublic Health Sciences Division, Program in Epidemiology, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Chu ChenPublic Health Sciences Division, Program in Epidemiology, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Gary GoodmanPublic Health Sciences Division, Cancer Prevention Program, Swedish Medical Center, Seattle, WA, USA.
Angela CoxDepartment of Oncology, University of Sheffield, Sheffield UK.
Fiona TaylorDepartment of Oncology, University of Sheffield, Sheffield UK.
Penella WollDepartment of Oncology, University of Sheffield, Sheffield UK.
H-Erich WichmannInstitute of Epidemiology, Helmholtz Centre Munich, Neuherberg, Germany.
Judith ManzInstitute of Epidemiology, Helmholtz Centre Munich, Neuherberg, Germany.
Thomas MuleyBiobank and Tumor Documentation, Thoraxklinik at University Hospital Heidelberg, Heidelberg, Germany.
Angela RischBiobank and Tumor Documentation, Thoraxklinik at University Hospital Heidelberg, Heidelberg, Germany.
Albert RosenbergerDepartment of Genetic Epidemiology, Medical School, Georg-August University of Göttingen, Göttingen, Germany.
Susanne M ArnoldMarkey Cancer Center, University of Kentucky, Lexington, KY, USA.
Eric B HauraDepartment of Thoracic Oncology, H. Lee Moffitt Cancer Center, Tampa, FL, USA.
Ciprian BolcaThoracic Surgery Division, "Marius Nasta" National Institute of Pneumology, Bucure?ti, Romania.
Ivana HolcatovaFaculty of Medicine, University of Ostrava, Ostrava, Czech Republic.
Vladimir JanoutFaculty of Medicine, University of Ostrava, Ostrava, Czech Republic.
Milica KonticInternal Medicine, School of Medicine, Clinical Center of Serbia, University of Belgrade, Belgrade, Serbia.
Jolanta LissowskaDepartment of Cancer Epidemiology and Prevention, M. Sklodowska-Curie Cancer Center, Institute of Oncology, Warsaw, Pol.
Anush MukeriaDepartment of Epidemiology and Prevention, Russian N.N. Blokhin Cancer Research Centre, Moscow, Russia.
Simona OgnjanovicInternational Organization for Cancer Prevention and Research, Belgrade, Serbia.
Tadeusz M OrlowskiDepartment of Thoracic Surgery, National Institute of Tuberculosis and Lung Diseases, Warsaw, Pol.
Ghislaine SceloInternational Agency for Research on Cancer (IARC), Genetic Epidemiology Group, Lyon, France.
Beata SwiatkowskaDepartment of Environmental Epidemiology, Nofer Institute of Occupational Medicine, Lódz, Pol.
David ZaridzeDepartment of Epidemiology and Prevention, Russian N.N. Blokhin Cancer Research Centre, Moscow, Russia.
Per BakkeDepartment of Clinical Science, University of Bergen, Bergen, Norway.
Vidar SkaugDepartment of Toxicology, National Institute of Occupational Health, Oslo, Norway.
Shanbeh ZienolddinyDepartment of Toxicology, National Institute of Occupational Health, Oslo, Norway.
Eric J DuellUnit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology (ICO-IDIBELL), Hospitalet de Llobregat, Barcelona, Spain.
Lesley M ButlerUniversity of Pittsburgh Cancer Institute, Pittsburgh, PA, USA.
Richard HoulstonThe Institute of Cancer Research, London, UK.
María Soler ArtigasDepartment of Health Sciences, Genetic Epidemiology Group, University of Leicester, Leicester, UK.
Kjell GrankvistDepartment of Medical Biosciences, Umeå University, Umeå, Sweden.
Mikael JohanssonDepartment of Radiation Sciences, Umeå University, Umeå, Sweden.
Frances A ShepherdMedical Oncology Toronto, Princess Margaret Hospital, Toronto, ON, Canada.
Michael W MarcusDepartment of Molecular and Clinical Cancer Medicine, University of Liverpool, Liverpool, UK.
Hans BrunnströmDepartment of Clinical Sciences, Lund University, Lund, Sweden.
Jonas ManjerDepartment of Internal Medicine, Skåne University Hospital, Malmö, Sweden.
Olle MelanderDepartment of Clinical Sciences, Lund University, Lund, Sweden.
David C MullerDepartment of Epidemiology and Biostatistics, Imperial College London, St Mary's Campus, London, UK.
Kim OvervadSection for Epidemiology, Department of Public Health, Aarhus University, Aarhus C, Denmark.
Antonia TrichopoulouDepartment of Hygiene and Epidemiology, Medical School, University of Athens, Athens, Greece.
Rosario TuminoMolecular and Nutritional Epidemiology Unit, CSPO (Cancer Research and Prevention Centre), Scientific Institute of Tuscany, Florence, Italy.
Geoffrey LiuPrincess Margaret Cancer Centre, Toronto, ON M5G, Canada.
Stig E BojesenDepartment of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Copenhagen, Denmark.
Xifeng WuDepartment of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
Loic Le MarchandEpidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
Demetrios AlbanesDivision of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institutes of Health, Bethesda, MD, USA.
Heike BickeböllerDepartment of Genetic Epidemiology, University Medical Center, Georg-August University Göttingen, Göttingen, Germany.
Melinda C AldrichDepartment of Thoracic Surgery, Division of Epidemiology, Vanderbilt University Medical Center, Nashville, TN, USA.
William S BushDepartment of Epidemiology and Biostatistics, School of Medicine, Case Western Reserve University, Cleveland, OH, USA.
Adonina TardonMedicina, IUOPA-Universidad de Oviedo, Oviedo, Spain.
Gad RennertTechnion Faculty of Medicine, Clalit National Cancer Control Center, Carmel Medical Center, Haifa, Israel.
M Dawn TeareGenetic Epidemiology, School of Health and Related Research, University of Sheffield, Sheffield, UK.
John K FieldInstitute of Translational Medicine, University of Liverpool, Liverpool, UK.
Lambertus A KiemeneyDepartment for Health Evidence, Radboud University Medical Center, Nijmegen EZ, Netherlands.
Philip LazarusDepartment of Pharmaceutical Sciences, College of Pharmacy, Washington State University, Spokane, WA, USA.
Aage HaugenDepartment of Toxicology, National Institute of Occupational Health, Oslo, Norway.
Stephen LamDepartment of Integrative Oncology, British Columbia Cancer Research Centre, Vancouver, BC, Canada.
Matthew B SchabathDepartment of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.
Angeline S AndrewDepartment of Epidemiology, Norris Cotton Cancer Center, Dartmouth College, Hanover, NH, USA.
Pier Alberto BertazziDepartment of Preventive Medicine, IRCCS Foundation Cà Granda Ospedale, Maggiore Policlinico, University of Milan, Milan, Italy.
Angela C PesatoriDepartment of Clinical Sciences and Community Health-DISCCO, University of Milan, Milan, Italy.
David C ChristianiDepartment of Epidemiology, Harvard School of Public Health, Boston, MA, USA.
Neil CaporasoDivision of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institutes of Health, Bethesda, MD, USA.
Mattias JohanssonInternational Agency for Research on Cancer, World Health Organization, Lyon, France.
James D McKayInternational Agency for Research on Cancer (IARC), Genetic Epidemiology Group, Lyon, France.
Paul BrennanInternational Agency for Research on Cancer, World Health Organization, Lyon, France.
Rayjean J HungDivision of Epidemiology, Dalla Lana School of Public Health, University of Toronto, Lunenfeld-Tanenbaum Research Institute, Toronto, Ontario, Canada.
Christopher I AmosBiomedical Data Science Department, Dartmouth College, Hanover, NH, USA.
Dartmouth College · USCentre international de recherche sur le cancer · FRUniversity of Sheffield · GBNational Institute of Occupational Health · NOFred Hutch Cancer Center · USHelmholtz Zentrum München · DELund University · SEMoffitt Cancer Center · USNational Institutes of Health · USPrincess Margaret Cancer Centre · CARussian Cancer Research Center NN Blokhin · RUUniversity of Göttingen · DEUniversity of Liverpool · GBUniversity of Milan · ITUniversity of Ostrava · CZAarhus University · DKCarmel Medical Center · ILCase Western Reserve University · USGentofte Hospital · DKHarvard University · US
Funding
TRANSLATIONAL RESEARCHP30CA076292 · NCI · UNIVERSITY OF SOUTH FLORIDA · PI John L. Cleveland · 1998 to 2026
$93.5MTranslational Engineering in Cancer (TEC)P30CA023108 · NCI · DARTMOUTH COLLEGE · PI Fred W Kolling IV · 1985 to 2026
$91.3MTranslating Molecular and Clinical Data to Population Lung Cancer Risk AssessmentU19CA203654 · NCI · UNIVERSITY OF NEW MEXICO HEALTH SCIS CTR · PI Christopher I. Amos, Rayjean J. Hung · 2017 to 2026
$23.7MAlpha-Tocopherol, Beta-Carotene Cancer Prevention (ATBC) StudyZIACP010195 · NCI · DIVISION OF CANCER EPIDEMIOLOGY AND GENETICS · PI ALBANES, DEMETRIUS · 2009 to 2025
$22.5MValidation of Biomarkers of Risk for the Early Detection of Lung CancerU01CA152662 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI DEPPEN, STEPHEN, GROGAN, ERIC L · 2010 to 2025
$12.8MThe Boston Lung Cancer Survival CohortU01CA209414 · NCI · HARVARD UNIVERSITY D/B/A HARVARD SCHOOL OF PUBLIC HEALTH · PI David C Christiani · 2017 to 2026
$12.2MSPORE in Lung CancerP50CA119997 · NCI · H. LEE MOFFITT CANCER CTR & RES INST · PI GABRILOVICH, DMITRY I · 2008 to 2012
$11.0MStatistical Methods for Analysis of Massive Genetic and Genomic Data in Cancer ResearchR35CA197449 · NCI · HARVARD UNIVERSITY D/B/A HARVARD SCHOOL OF PUBLIC HEALTH · PI XIHONG LIN · 2015 to 2026
$10.9MTransdisciplinary Research in Cancer of the Lung (TRICL)U19CA148127 · NCI · UNIVERSITY OF TX MD ANDERSON CAN CTR · PI AMOS, CHRISTOPHER I., LE MARCHAND, LOIC · 2010 to 2014
$10.9MInfrastructure Support and Pilot Tissue Collection for the CARET BiorepositoryU01CA167462 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI NEUHOUSER, MARIAN L · 2018 to 2022
$2.9MUnraveling Genetic Determinants of Lung Cancer Risk in African AmericansK07CA172294 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI ALDRICH, MELINDA · 2013 to 2017
$801kCancer Research UK 20622NCI NIH HHS K07 CA172294NCI NIH HHS P30 CA023108NCI NIH HHS P30 CA076292NCI NIH HHS P50 CA119997NCI NIH HHS R35 CA197449NCI NIH HHS U01 CA152662NCI NIH HHS U01 CA167462NCI NIH HHS U01 CA209414NCI NIH HHS U19 CA148127NCI NIH HHS U19 CA203654World Health Organization 001
Abstract
Non-small cell lung cancer is the most common type of lung cancer. Both environmental and genetic risk factors contribute to lung carcinogenesis. We conducted a genome-wide interaction analysis between single nucleotide polymorphisms (SNPs) and smoking status (never- versus ever-smokers) in a European-descent population. We adopted a two-step analysis strategy in the discovery stage: we first conducted a case-only interaction analysis to assess the relationship between SNPs and smoking behavior using 13336 non-small cell lung cancer cases. Candidate SNPs with P-value <0.001 were further analyzed using a standard case-control interaction analysis including 13970 controls. The significant SNPs with P-value <3.5 × 10-5 (correcting for multiple tests) from the case-control analysis in the discovery stage were further validated using an independent replication dataset comprising 5377 controls and 3054 non-small cell lung cancer cases. We further stratified the analysis by histological subtypes. Two novel SNPs, rs6441286 and rs17723637, were identified for overall lung cancer risk. The interaction odds ratio and meta-analysis P-value for these two SNPs were 1.24 with 6.96 × 10-7 and 1.37 with 3.49 × 10-7, respectively. In addition, interaction of smoking with rs4751674 was identified in squamous cell lung carcinoma with an odds ratio of 0.58 and P-value of 8.12 × 10-7. This study is by far the largest genome-wide SNP-smoking interaction analysis reported for lung cancer. The three identified novel SNPs provide potential candidate biomarkers for lung cancer risk screening and intervention. The results from our study reinforce that gene-smoking interactions play important roles in the etiology of lung cancer and account for part of the missing heritability of this disease.
Indexed as
Carcinoma, Non-Small-Cell LungCase-Control StudiesGene-Environment InteractionGenetic Predisposition to DiseaseGenome-Wide Association StudyGenotypeHumansLung NeoplasmsPolymorphism, Single NucleotideSmokingWhite People
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