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      Genome-wide association study of lung adenocarcinoma in East Asia and comparison with a European population

      research-article
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      Nature Communications
      Nature Publishing Group UK
      Genome-wide association studies, Cancer epidemiology

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          Abstract

          Lung adenocarcinoma is the most common type of lung cancer. Known risk variants explain only a small fraction of lung adenocarcinoma heritability. Here, we conducted a two-stage genome-wide association study of lung adenocarcinoma of East Asian ancestry (21,658 cases and 150,676 controls; 54.5% never-smokers) and identified 12 novel susceptibility variants, bringing the total number to 28 at 25 independent loci. Transcriptome-wide association analyses together with colocalization studies using a Taiwanese lung expression quantitative trait loci dataset ( n = 115) identified novel candidate genes, including FADS1 at 11q12 and ELF5 at 11p13. In a multi-ancestry meta-analysis of East Asian and European studies, four loci were identified at 2p11, 4q32, 16q23, and 18q12. At the same time, most of our findings in East Asian populations showed no evidence of association in European populations. In our studies drawn from East Asian populations, a polygenic risk score based on the 25 loci had a stronger association in never-smokers vs. individuals with a history of smoking (P interaction = 0.0058). These findings provide new insights into the etiology of lung adenocarcinoma in individuals from East Asian populations, which could be important in developing translational applications.

          Abstract

          Genome-wide association studies (GWAS) have improved our understanding of the genetic basis of lung adenocarcinoma but known susceptibility variants explain only a small fraction of the familial risk. Here, the authors perform a two-stage GWAS and report 12 novel genetic loci associated with lung adenocarcinoma in East Asians.

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          Most cited references84

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          • Abstract: found
          • Article: not found

          Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries

          This article provides a status report on the global burden of cancer worldwide using the GLOBOCAN 2018 estimates of cancer incidence and mortality produced by the International Agency for Research on Cancer, with a focus on geographic variability across 20 world regions. There will be an estimated 18.1 million new cancer cases (17.0 million excluding nonmelanoma skin cancer) and 9.6 million cancer deaths (9.5 million excluding nonmelanoma skin cancer) in 2018. In both sexes combined, lung cancer is the most commonly diagnosed cancer (11.6% of the total cases) and the leading cause of cancer death (18.4% of the total cancer deaths), closely followed by female breast cancer (11.6%), prostate cancer (7.1%), and colorectal cancer (6.1%) for incidence and colorectal cancer (9.2%), stomach cancer (8.2%), and liver cancer (8.2%) for mortality. Lung cancer is the most frequent cancer and the leading cause of cancer death among males, followed by prostate and colorectal cancer (for incidence) and liver and stomach cancer (for mortality). Among females, breast cancer is the most commonly diagnosed cancer and the leading cause of cancer death, followed by colorectal and lung cancer (for incidence), and vice versa (for mortality); cervical cancer ranks fourth for both incidence and mortality. The most frequently diagnosed cancer and the leading cause of cancer death, however, substantially vary across countries and within each country depending on the degree of economic development and associated social and life style factors. It is noteworthy that high-quality cancer registry data, the basis for planning and implementing evidence-based cancer control programs, are not available in most low- and middle-income countries. The Global Initiative for Cancer Registry Development is an international partnership that supports better estimation, as well as the collection and use of local data, to prioritize and evaluate national cancer control efforts. CA: A Cancer Journal for Clinicians 2018;0:1-31. © 2018 American Cancer Society.
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            • Article: not found

            Detection of widespread horizontal pleiotropy in causal relationships inferred from Mendelian randomization between complex traits and diseases

            Horizontal pleiotropy occurs when the variant has an effect on disease outside of its effect on the exposure in Mendelian randomization (MR). Violation of the ‘no horizontal pleiotropy’ assumption can cause severe bias in MR. We developed the Mendelian Randomization Pleiotropy RESidual Sum and Outlier (MR-PRESSO) test to identify horizontal pleiotropic outliers in multi-instrument summary-level MR testing. We showed using simulations that MR-PRESSO is best suited when horizontal pleiotropy occurs in <50% of instruments. Next, we applied MR-PRESSO, along with several other MR tests to complex traits and diseases, and found that horizontal pleiotropy: (i) was detectable in over 48% of significant causal relationships in MR; (ii) introduced distortions in the causal estimates in MR that ranged on average from −131% to 201%; (iii) induced false positive causal relationships in up to 10% of relationships; and (iv) can be corrected in some but not all instances.
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              • Record: found
              • Abstract: found
              • Article: not found

              An Atlas of Genetic Correlations across Human Diseases and Traits

              Identifying genetic correlations between complex traits and diseases can provide useful etiological insights and help prioritize likely causal relationships. The major challenges preventing estimation of genetic correlation from genome-wide association study (GWAS) data with current methods are the lack of availability of individual genotype data and widespread sample overlap among meta-analyses. We circumvent these difficulties by introducing a technique – cross-trait LD Score regression – for estimating genetic correlation that requires only GWAS summary statistics and is not biased by sample overlap. We use this method to estimate 276 genetic correlations among 24 traits. The results include genetic correlations between anorexia nervosa and schizophrenia, anorexia and obesity and associations between educational attainment and several diseases. These results highlight the power of genome-wide analyses, since there currently are no significantly associated SNPs for anorexia nervosa and only three for educational attainment.
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                Author and article information

                Contributors
                jianxin.shi@nih.gov
                qingl@mail.nih.gov
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                26 May 2023
                26 May 2023
                2023
                : 14
                : 3043
                Affiliations
                [1 ]GRID grid.48336.3a, ISNI 0000 0004 1936 8075, Division of Cancer Epidemiology and Genetics, , National Cancer Institute, ; Rockville, MD USA
                [2 ]GRID grid.272242.3, ISNI 0000 0001 2168 5385, Division of Genome Biology, , National Cancer Research Institute, ; Tokyo, Japan
                [3 ]GRID grid.410800.d, ISNI 0000 0001 0722 8444, Division of Cancer Epidemiology and Prevention, , Aichi Cancer Center Research Institute, ; Nagoya, Japan
                [4 ]GRID grid.59784.37, ISNI 0000000406229172, Institute of Population Health Sciences, , National Health Research Institutes, ; Zhunan, Taiwan
                [5 ]GRID grid.89957.3a, ISNI 0000 0000 9255 8984, Department of Epidemiology, School of Public Health, , Nanjing Medical University, ; Nanjing, China
                [6 ]GRID grid.89957.3a, ISNI 0000 0000 9255 8984, Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Medicine, , Nanjing Medical University, ; Nanjing, China
                [7 ]GRID grid.250674.2, ISNI 0000 0004 0626 6184, Prosserman Centre for Population Health Research, , Lunenfeld-Tanenbaum Research Institute, Sinai Health, ; Toronto, ON Canada
                [8 ]Department of Epidemiology and Biostatistics, National Clinical Research Center for Cancer, Key Laboratory of Molecular Cancer Epidemiology of Tianjin, Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University, Tianjin, China
                [9 ]GRID grid.412807.8, ISNI 0000 0004 1936 9916, Division of Epidemiology, Department of Medicine, , Vanderbilt University Medical Center and Vanderbilt-Ingram Cancer Center, ; Nashville, TN USA
                [10 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Cancer Research Institute, , Seoul National University College of Medicine, ; Seoul, Republic of Korea
                [11 ]GRID grid.506261.6, ISNI 0000 0001 0706 7839, Department of Etiology & Carcinogenesis and State Key Laboratory of Molecular Oncology, Cancer Institute and Hospital, , Chinese Academy of Medical Sciences and Peking Union Medical College, ; Beijing, China
                [12 ]GRID grid.412449.e, ISNI 0000 0000 9678 1884, Department of Epidemiology, School of Public Health, , China Medical University, ; Shenyang, China
                [13 ]GRID grid.412636.4, ISNI 0000 0004 1757 9485, Department of Clinical Epidemiology and Center of Evidence Based Medicine, , The First Hospital of China Medical University, ; Shenyang, China
                [14 ]GRID grid.410587.f, Department of Oncology, Shandong Cancer Hospital and Institute, , Shandong Academy of Medical Sciences, ; Jinan, China
                [15 ]GRID grid.8547.e, ISNI 0000 0001 0125 2443, Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, , Fudan University, ; Shanghai, China
                [16 ]GRID grid.8547.e, ISNI 0000 0001 0125 2443, State Key Laboratory of Genetic Engineering, School of Life Sciences, , Fudan University, ; Shanghai, China
                [17 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Saw Swee Hock School of Public Health, National University of Singapore, ; Singapore, Singapore
                [18 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Department of Medicine, Yong Loo Lin School of Medicine, , National University of Singapore and National University Health System, ; Singapore, Singapore
                [19 ]GRID grid.59784.37, ISNI 0000000406229172, National Institute of Cancer Research, , National Health Research Institutes, ; Zhunan, Taiwan
                [20 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Department of Preventive Medicine, , Seoul National University College of Medicine, ; Seoul, Republic of Korea
                [21 ]GRID grid.14005.30, ISNI 0000 0001 0356 9399, Department of Preventive Medicine, , Chonnam National University Medical School, ; Gwangju, Republic of Korea
                [22 ]GRID grid.410643.4, Guangdong Lung Cancer Institute, Medical Research Center and Cancer Center of Guangdong Provincial People’s Hospital, , Guangdong Academy of Medical Sciences, ; Guangzhou, China
                [23 ]GRID grid.415550.0, ISNI 0000 0004 1764 4144, Department of Pathology, , Queen Mary Hospital, ; Hong Kong, Hong Kong
                [24 ]GRID grid.10698.36, ISNI 0000000122483208, Department of Biostatistics, , Gillings School of Global Public Health, University of North Carolina, ; Chapel Hill, NC USA
                [25 ]GRID grid.411667.3, ISNI 0000 0001 2186 0438, Department of Biostatistics, Bioinformatics & Biomathematics, , Georgetown University Medical Center, ; Washington, DC USA
                [26 ]GRID grid.240871.8, ISNI 0000 0001 0224 711X, Department of Computational Biology, , St. Jude Children’s Research Hospital, ; Memphis, TN USA
                [27 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Department of Environmental Health, Graduate School of Public Health, , Seoul National University, ; Seoul, Republic of Korea
                [28 ]GRID grid.412532.3, Shanghai Pulmonary Hospital, ; Shanghai, China
                [29 ]GRID grid.272242.3, ISNI 0000 0001 2168 5385, Department of Pathology and Clinical Laboratories, , National Cancer Center Hospital, ; Tokyo, Japan
                [30 ]GRID grid.411602.0, ISNI 0000 0004 0647 9534, Lung and Esophageal Cancer Clinic, , Chonnam National University Hwasun Hospital, ; Hwasuneup, Republic of Korea
                [31 ]GRID grid.14005.30, ISNI 0000 0001 0356 9399, Department of Internal Medicine, , Chonnam National Univerisity Medical School, ; Gwangju, Republic of Korea
                [32 ]GRID grid.506261.6, ISNI 0000 0001 0706 7839, Department of Etiology & Carcinogenesis, Cancer Institute and Hospital, , Chinese Academy of Medical Sciences and Peking Union Medical College, ; Beijing, China
                [33 ]GRID grid.415550.0, ISNI 0000 0004 1764 4144, Department of Medicine, , The University of Hong Kong, Queen Mary Hospital, ; Hong Kong, Hong Kong
                [34 ]GRID grid.509459.4, ISNI 0000 0004 0472 0267, Laboratory for Genotyping Development, , RIKEN Center for Integrative Medical Sciences, ; Yokohama, Japan
                [35 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Center for Antibody and Vaccine Therapy, Research Hospital, Institute of Medical Science, , The University of Tokyo, ; Tokyo, Japan
                [36 ]GRID grid.410827.8, ISNI 0000 0000 9747 6806, Department of Medical Oncology and Cancer Center, and Center for Advanced Medicine against Cancer, , Shiga University of Medical Science, ; Shiga, Japan
                [37 ]GRID grid.412670.6, ISNI 0000 0001 0729 3748, Department of Statistics & Research Institute of Natural Sciences, , Sookmyung Women’s University, ; Seoul, Republic of Korea
                [38 ]GRID grid.509459.4, ISNI 0000 0004 0472 0267, Laboratory for Statistical Analysis, , RIKEN Center for Integrative Medical Sciences, ; Yokohama, Japan
                [39 ]GRID grid.265073.5, ISNI 0000 0001 1014 9130, Department of Thoracic Surgery, , Tokyo Medical and Dental University, ; Tokyo, Japan
                [40 ]GRID grid.265073.5, ISNI 0000 0001 1014 9130, Department of Respiratory Medicine, , Tokyo Medical and Dental University, ; Tokyo, Japan
                [41 ]GRID grid.251993.5, ISNI 0000000121791997, Department of Epidemiology and Population Health, , Albert Einstein College of Medicine, ; New York, NY USA
                [42 ]GRID grid.414929.3, ISNI 0000 0004 1763 7921, Department of Medical Oncology, , Japanese Red Cross Medical Center, ; Tokyo, Japan
                [43 ]GRID grid.272242.3, ISNI 0000 0001 2168 5385, Department of Thoracic Surgery, , National Cancer Center Hospital, ; Tokyo, Japan
                [44 ]GRID grid.414944.8, ISNI 0000 0004 0629 2905, Molecular Pathology and Genetics Division, , Kanagawa Cancer Center Research Institute, ; Yokohama, Japan
                [45 ]GRID grid.414944.8, ISNI 0000 0004 0629 2905, Department of Thoracic Surgery, , Kanagawa Cancer Center, ; Yokohama, Japan
                [46 ]GRID grid.497282.2, Department of Thoracic Oncology, , National Cancer Center Hospital East, ; Kashiwa, Japan
                [47 ]GRID grid.497282.2, Department of Thoracic Surgery, , National Cancer Center Hospital East, ; Kashiwa, Japan
                [48 ]GRID grid.272242.3, ISNI 0000 0001 2168 5385, Division of Medical AI Research and Development, , National Cancer Center Research Institute, ; Tokyo, Japan
                [49 ]GRID grid.251924.9, ISNI 0000 0001 0725 8504, Department of Cellular and Organ Pathology, , Graduate School of Medicine, Akita University, ; Akita, Japan
                [50 ]GRID grid.251924.9, ISNI 0000 0001 0725 8504, Department of Thoracic Surgery, , Graduate School of Medicine, Akita University, ; Akita, Japan
                [51 ]GRID grid.412339.e, ISNI 0000 0001 1172 4459, Department of Preventive Medicine, Faculty of Medicine, , Saga University, ; Saga, Japan
                [52 ]GRID grid.27476.30, ISNI 0000 0001 0943 978X, Department of Preventive Medicine, , Nagoya University Graduate School of Medicine, ; Nagoya, Japan
                [53 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Laboratory of Clinical Genome Sequencing, Department of Computational Biology and Medical Science, Graduate School of Frontier Sciences, , The University of Tokyo, ; Tokyo, Japan
                [54 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Division of Molecular Pathology, Institute of Medical Science, , The University of Tokyo, ; Tokyo, Japan
                [55 ]GRID grid.263518.b, ISNI 0000 0001 1507 4692, Department of Surgery, Division of General Thoracic Surgery, , Shinshu University School of Medicine Asahi, ; Nagano, Japan
                [56 ]GRID grid.411582.b, ISNI 0000 0001 1017 9540, Department of Chest Surgery, , Fukushima Medical University School of Medicine, ; Fukushima, Japan
                [57 ]GRID grid.411582.b, ISNI 0000 0001 1017 9540, Department of Gastrointestinal Tract Surgery, , Fukushima Medical University School of Medicine, ; Fukushima, Japan
                [58 ]GRID grid.411887.3, ISNI 0000 0004 0595 7039, Department of Integrative center of General Surgery, , Gunma University Hospital, ; Gunma, Japan
                [59 ]GRID grid.33199.31, ISNI 0000 0004 0368 7223, Institute of Occupational Medicine and Ministry of Education Key Lab for Environment and Health, School of Public Health, , Huazhong University of Science and Technology, ; Wuhan, China
                [60 ]GRID grid.464219.c, ISNI 0000 0004 0574 7605, China National Environmental Monitoring Center, ; Beijing, China
                [61 ]GRID grid.411134.2, ISNI 0000 0004 0474 0479, Department of Internal Medicine, Division of Oncology/Hematology, College of Medicine, , Korea University Anam Hospital, ; Seoul, Republic of Korea
                [62 ]GRID grid.415550.0, ISNI 0000 0004 1764 4144, Department of Clinical Oncology, , The University of Hong Kong, Queen Mary Hospital, ; Hong Kong, Hong Kong
                [63 ]GRID grid.411641.7, ISNI 0000 0004 0532 2041, School of Medicine and Institute of Medicine, , Chung Shan Medical University, ; Taichung, Taiwan
                [64 ]GRID grid.411645.3, ISNI 0000 0004 0638 9256, Department of Internal Medicine, Division of Pulmonary Medicine, , Chung Shan Medical University Hospital, ; Taichung, Taiwan
                [65 ]GRID grid.260542.7, ISNI 0000 0004 0532 3749, Institute of Biomedical Sciences, , National Chung Hsing University, ; Taichung, Taiwan
                [66 ]GRID grid.410764.0, ISNI 0000 0004 0573 0731, Department of Internal Medicine, , Division of Chest Medicine, Taichung Veterans General Hospital, ; Taichung, Taiwan
                [67 ]GRID grid.145695.a, ISNI 0000 0004 1798 0922, Department of Respiratory Therapy, , Chang Gung University, ; Taoyuan, Taiwan
                [68 ]GRID grid.508002.f, ISNI 0000 0004 1777 8409, Department of Pulmonary and Critical Care, , Xiamen Chang Gung Hospital, ; Xiamen, China
                [69 ]GRID grid.412094.a, ISNI 0000 0004 0572 7815, Department of Internal Medicine, , National Taiwan University Hospital and College of Medicine, ; Taipei, Taiwan
                [70 ]GRID grid.412019.f, ISNI 0000 0000 9476 5696, Department of Internal Medicine, , E-Da Cancer Hospital, I-Shou University and Kaohsiung Medical University, ; Kaohsiung, Taiwan
                [71 ]GRID grid.412040.3, ISNI 0000 0004 0639 0054, Department of Oncology, , National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, ; Tainan, Taiwan
                [72 ]GRID grid.278247.c, ISNI 0000 0004 0604 5314, Department of Chest Medicine, , Taipei Veterans General Hospital, and school of Medicine, National Yang Ming Chiao Tung University, ; Taipei, Taiwan
                [73 ]GRID grid.477473.4, Lung Cancer Center, , Kyungpook National University Medical Center, ; Daegu, Republic of Korea
                [74 ]GRID grid.14005.30, ISNI 0000 0001 0356 9399, Jeonnam Regional Cancer Center, , Chonnam National University, ; Hwasun, Republic of Korea
                [75 ]GRID grid.419087.3, ISNI 0000 0004 1789 563X, Department of Epidemiology, , Shanghai Cancer Institute, ; Shanghai, China
                [76 ]GRID grid.185448.4, ISNI 0000 0004 0637 0221, Genome Institute of Singapore, Agency of Science, , Technology and Research, ; Singapore, Singapore
                [77 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Yong Loo Lin School of Medicine, , National University of Singapore, ; Singapore, Singapore
                [78 ]GRID grid.477517.7, ISNI 0000 0004 0396 4462, Karmanos Cancer Institute, ; Detroit, MI USA
                [79 ]GRID grid.18886.3f, Division of Genetics and Epidemiology, , Institute of Cancer Research, ; London, UK
                [80 ]Department of Medicine, Section of Epidemiology and Population Science, Institute for Clinical and Translational Research, Houston, TX USA
                [81 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, School of Medicine, , Zhejiang University, ; Hangzhou, Zhejiang China
                [82 ]GRID grid.417468.8, ISNI 0000 0000 8875 6339, Department of Health Sciences Research, , Mayo Clinic, ; Scottsdale, AZ USA
                [83 ]GRID grid.248762.d, ISNI 0000 0001 0702 3000, British Columbia Cancer Agency, ; Vancouver, BC Canada
                [84 ]GRID grid.10863.3c, ISNI 0000 0001 2164 6351, IUOPA, , University of Oviedo and CIBERESP, ; Madrid, Spain
                [85 ]GRID grid.270240.3, ISNI 0000 0001 2180 1622, Public Health Sciences Division, , Fred Hutchinson Cancer Center, ; Seattle, WA USA
                [86 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Faculty of Health and Medical Sciences, , University of Copenhagen, ; Copenhagen, Denmark
                [87 ]GRID grid.4973.9, ISNI 0000 0004 0646 7373, Department of Clinical Biochemistry, Herlev and Gentofte Hospital, , Copenhagen University Hospital, ; Copenhagen, Denmark
                [88 ]GRID grid.17703.32, ISNI 0000000405980095, International Agency for Research on Cancer (IARC/WHO), ; Lyon, France
                [89 ]GRID grid.7497.d, ISNI 0000 0004 0492 0584, German Cancer Research Center (DKFZ), ; Heidelberg, Germany
                [90 ]GRID grid.5253.1, ISNI 0000 0001 0328 4908, Translational Lung Research Center Heidelberg (TLRC-H), , Member of the German Center for Lung Research (DZL), ; Heidelberg, Germany
                [91 ]GRID grid.7039.d, ISNI 0000000110156330, University of Salzburg and Cancer Cluster Salzburg, ; Salzburg, Austria
                [92 ]GRID grid.411984.1, ISNI 0000 0001 0482 5331, University Medical Center Goettingen, ; Goettingen, Germany
                [93 ]GRID grid.5252.0, ISNI 0000 0004 1936 973X, Institute of Medical Informatics, Biometry and Epidemiology, , Ludwig Maximilians University, ; Munich, Germany
                [94 ]GRID grid.4567.0, ISNI 0000 0004 0483 2525, Helmholtz Center Munich, , Institute of Epidemiology, ; Munich, Germany
                [95 ]GRID grid.6936.a, ISNI 0000000123222966, Institute of Medical Statistics and Epidemiology, , Technical University Munich, ; Munich, Germany
                [96 ]GRID grid.38142.3c, ISNI 000000041936754X, Harvard TH Chan School of Public Health, ; Boston, MA USA
                [97 ]GRID grid.413469.d, Carmel Medical Center, ; Haifa, Israel
                [98 ]GRID grid.478547.d, ISNI 0000 0004 0402 4587, Markey Cancer Center, ; Lexington, KY USA
                [99 ]GRID grid.10025.36, ISNI 0000 0004 1936 8470, Liverpool University, ; Liverpool, UK
                [100 ]GRID grid.240145.6, ISNI 0000 0001 2291 4776, The University of Texas MD Anderson Cancer Center, ; Houston, TX USA
                [101 ]GRID grid.516097.c, ISNI 0000 0001 0311 6891, Epidemiology Program, , University of Hawaii Cancer Center, ; Honolulu, HI USA
                [102 ]GRID grid.415224.4, ISNI 0000 0001 2150 066X, Princess Margaret Cancer Center, ; Toronto, ON Canada
                [103 ]GRID grid.516082.8, ISNI 0000 0000 9476 9750, Norris Cotton Cancer Center, ; Lebanon, NH USA
                [104 ]GRID grid.10417.33, ISNI 0000 0004 0444 9382, Radboud University Medical Center, ; Nijmegen, Netherlands
                [105 ]GRID grid.416876.a, ISNI 0000 0004 0630 3985, National Institute of Occupational Health, ; Oslo, Norway
                [106 ]GRID grid.12650.30, ISNI 0000 0001 1034 3451, Department of Medical Biosciences, , Umeå University, ; Umeå, Sweden
                [107 ]GRID grid.12650.30, ISNI 0000 0001 1034 3451, Department of Radiation Sciences, , Umeå University, ; Umeå, Sweden
                [108 ]GRID grid.11835.3e, ISNI 0000 0004 1936 9262, University of Sheffield, ; Sheffield, UK
                [109 ]GRID grid.21925.3d, ISNI 0000 0004 1936 9000, UPMC Hillman Cancer Center and Department of Epidemiology, School of Public Health, , University of Pittsburgh, ; Pittsburgh, PA USA
                [110 ]GRID grid.470982.0, ISNI 0000 0004 0400 6231, Washington State University College of Pharmacy, ; Spokane, WA USA
                [111 ]GRID grid.468198.a, ISNI 0000 0000 9891 5233, Department of Cancer Epidemiology, , H. Lee Moffitt Cancer Center and Research Institute, ; Tampa, FL USA
                [112 ]GRID grid.412807.8, ISNI 0000 0004 1936 9916, Department of Thoracic Surgery, Division of Epidemiology, , Vanderbilt University Medical Center, ; Nashville, TN USA
                [113 ]GRID grid.477473.4, Cancer Research Center, , Kyungpook National University Medical Center, ; Daegu, Republic of Korea
                [114 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Department of Thoracic and Cardiovascular Surgery, Cancer Research Institute, , Seoul National University College of Medicine, ; Seoul, Republic of Korea
                [115 ]GRID grid.33199.31, ISNI 0000 0004 0368 7223, Department of Occupational and Environmental Health and Ministry of Education Key Lab for Environment and Health, School of Public Health, Tongji Medical College, , Huazhong University of Science and Technology, ; Wuhan, China
                [116 ]GRID grid.419407.f, ISNI 0000 0004 4665 8158, Cancer Genomics Research Laboratory, , Leidos Biomedical Research Inc., ; Rockville, MD USA
                [117 ]GRID grid.194645.b, ISNI 0000000121742757, Department of Biochemistry, Li Ka Shing (LKS) Faculty of Medicine, , The University of Hong Kong, ; Hong Kong, China
                [118 ]GRID grid.194645.b, ISNI 0000000121742757, Centre for Genomic Sciences, Li Ka Shing (LKS) Faculty of Medicine, , The University of Hong Kong, ; Hong Kong, China
                [119 ]GRID grid.418377.e, ISNI 0000 0004 0620 715X, Department of Human Genetics, , Genome Institute of Singapore, ; Singapore, Singapore
                [120 ]GRID grid.412480.b, ISNI 0000 0004 0647 3378, Department of Thoracic and Cardiovascular Surgery, , Seoul National University Bundang Hospital, ; Seongnam, Republic of Korea
                [121 ]GRID grid.33199.31, ISNI 0000 0004 0368 7223, Department of Oncology, Cancer Center, Union Hospital, , Huazhong University of Science and Technology, ; Wuhan, China
                [122 ]GRID grid.412896.0, ISNI 0000 0000 9337 0481, The Ph.D. Program for Translational Medicine, College of Medical Science and Technology, , Taipei Medical University, ; Taipei, Taiwan
                [123 ]GRID grid.194645.b, ISNI 0000000121742757, School of Public Health, Li Ka Shing (LKS) Faculty of Medicine, , The University of Hong Kong, ; Hong Kong, China
                [124 ]GRID grid.411356.4, ISNI 0000 0000 9339 3042, Key Laboratory of Cancer Etiology and Intervention, , University of Liaoning Province, ; Shenyang, China
                [125 ]GRID grid.412094.a, ISNI 0000 0004 0572 7815, Department of Internal Medicine, , National Taiwan University Hospital Hsin-Chu Branch, ; Hsinchu, Taiwan
                [126 ]Gleneagles Hong Kong Hospital, Hong Kong, China
                [127 ]GRID grid.411134.2, ISNI 0000 0004 0474 0479, Department of Internal Medicine, Division of Medical Oncology, College of Medicine, , Korea University Guro Hospital, ; Seoul, Republic of Korea
                [128 ]GRID grid.412480.b, ISNI 0000 0004 0647 3378, Department of Internal Medicine, , Seoul National University Bundang Hospital, ; Seongnam, Republic of Korea
                [129 ]Department of Oncology, Wuhan Iron and Steel (Group) Corporation Staff-Worker Hospital, Wuhan, China
                [130 ]GRID grid.413801.f, ISNI 0000 0001 0711 0593, Department of Pulmonary and Critical Care, , Chang Gung Memorial Hospital, ; Taoyuan, Taiwan
                [131 ]GRID grid.5477.1, ISNI 0000000120346234, Division of Environmental Epidemiology, Institute for Risk Assessment Sciences (IRAS), , Utrecht University, ; Utrecht, The Netherlands
                [132 ]GRID grid.266102.1, ISNI 0000 0001 2297 6811, Department of Epidemiology and Biostatistics, , University of California, San Francisco, ; San Francisco, CA USA
                [133 ]GRID grid.415499.4, ISNI 0000 0004 1771 451X, Department of Pathology, , Queen Elizabeth Hospital, ; Hong Kong, China
                [134 ]Qujing Center for Diseases Control and Prevention, Qujing, China
                [135 ]GRID grid.272242.3, ISNI 0000 0001 2168 5385, Division of Cohort Research, National Cancer Center Institute for Cancer Control, , National Cancer Center, ; Tokyo, Japan
                [136 ]GRID grid.272242.3, ISNI 0000 0001 2168 5385, Division of Epidemiology, National Cancer Center Institute for Cancer Control, , National Cancer Center, ; Tokyo, Japan
                [137 ]GRID grid.48336.3a, ISNI 0000 0004 1936 8075, Center for Global Health, , National Cancer Institute, ; Bethesda, MD USA
                [138 ]GRID grid.411641.7, ISNI 0000 0004 0532 2041, Institute of Medicine, , Chung Shan Medical University, ; Taichung, Taiwan
                [139 ]GRID grid.411645.3, ISNI 0000 0004 0638 9256, Division of Thoracic Surgery, Department of Surgery, , Chung Shan Medical University Hospital, ; Taichung, Taiwan
                [140 ]GRID grid.28665.3f, ISNI 0000 0001 2287 1366, Genomic Research Center, , Academia Sinica, ; Taipei, Taiwan
                [141 ]GRID grid.412094.a, ISNI 0000 0004 0572 7815, Department of Internal Medicine, , National Taiwan University Hospital, ; Taipei, Taiwan
                [142 ]GRID grid.422418.9, ISNI 0000 0004 0371 6485, Laboratory Services, , American Cancer Society, ; Atlanta, GA USA
                [143 ]GRID grid.21107.35, ISNI 0000 0001 2171 9311, Department of Oncology, School of Medicine, , Johns Hopkins University, ; Baltimore, MD USA
                [144 ]GRID grid.21107.35, ISNI 0000 0001 2171 9311, Department of Biostatistics, , Johns Hopkins Bloomberg School of Public Health, ; Baltimore, MD USA
                [145 ]GRID grid.516068.c, Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, ; Houston, TX USA
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                Article
                38196
                10.1038/s41467-023-38196-z
                10220065
                37236969
                72aa128e-f8d3-423e-80c9-28e09c625072
                © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2023

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                History
                : 27 February 2022
                : 19 April 2023
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                genome-wide association studies,cancer epidemiology
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                genome-wide association studies, cancer epidemiology

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