Evidence map›Paper›PMID 36539618›Full record

SynthesisNature genetics2023

Deciphering colorectal cancer genetics through multi-omic analysis of 100,204 cases and 154,587 controls of European and east Asian ancestries.

Ceres Fernandez-Rozadilla, Maria Timofeeva, Zhishan Chen, Philip Law, Minta Thomas, Stephanie Schmit, Virginia Díez-Obrero, Li Hsu, Juan Fernandez-Tajes, Claire Palles and 200 more

Erratum issuedOpen access · greenAbstract readMeta-Analysis
PubMed Full text at PMC Publisher
In one paragraph

Synthesis in Nature genetics, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 162 papers, 7 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
162citing papers in PubMed, 7 pooled it
31.6field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

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.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

162 citing papers in PubMed, 7 syntheses or guidelines pooled it, 227 citations in OpenAlex.

  1. Pooled it
  2. Pooled it
  3. Pooled it
  4. Pooled it
  5. Pooled it
  6. Genome-wide association studies and Mendelian randomization analyses provide insights into the causes of early-onset colorectal cancer.Annals of oncology : official journal of the European Society for Medical Oncology · 2024
    Pooled it
  7. Genome-Wide Association and Two-Sample Mendelian Randomization Analyses of Plasma Ghrelin and Gastrointestinal Cancer Risk.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2023
    Pooled it
  8. Review
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  12. Review
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  16. Emerging trends in the global burden of colorectal cancer.Nature reviews. Clinical oncology · 2026
    Review
  17. Article
  18. Article
  19. Article
  20. Article

102 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

210 authors at 20 institutions in 24 countries.

Ceres Fernandez-Rozadilla *Edinburgh Cancer Research Centre, Institute of Genomics and Cancer, University of Edinburgh, Edinburgh, UK.ORCID 0000-0001-7330-4804
Maria Timofeeva *Colon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.ORCID 0000-0002-2503-4253
Zhishan Chen *Division of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.
Philip Law *Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.ORCID 0000-0001-9663-4611
Minta Thomas *Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0001-9337-7015
Stephanie Schmit *Genomic Medicine Institute, Cleveland Clinic, Cleveland, OH, USA.ORCID 0000-0001-5931-1194
Virginia Díez-Obrero *Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute, Barcelona, Spain.
Li Hsu *Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Juan Fernandez-TajesEdinburgh Cancer Research Centre, Institute of Genomics and Cancer, University of Edinburgh, Edinburgh, UK.
Claire PallesInstitute of Cancer and Genomic Sciences, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.ORCID 0000-0002-9670-2263
Kitty SherwoodEdinburgh Cancer Research Centre, Institute of Genomics and Cancer, University of Edinburgh, Edinburgh, UK.
Sarah BriggsDepartment of Public Health, Richard Doll Building, University of Oxford, Oxford, UK.
Victoria SvintiColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.
Kevin DonnellyColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.
Susan FarringtonColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.ORCID 0000-0001-5955-7389
James BlackmurColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.
Peter Vaughan-ShawColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.
Xiao-Ou ShuDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.
Jirong LongDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.
Qiuyin CaiDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.
Xingyi GuoDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.ORCID 0000-0001-5269-1294
Yingchang LuDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.
Peter BroderickDivision of Genetics and Epidemiology, Institute of Cancer Research, London, UK.ORCID 0000-0002-8348-5829
James StuddDivision of Genetics and Epidemiology, Institute of Cancer Research, London, UK.ORCID 0000-0002-7157-754X
Jeroen HuyghePublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0001-6027-9806
Tabitha HarrisonPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0002-4173-7530
David ContiDepartment of Preventive Medicine, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Christopher DampierCenter for Public Health Genomics, Department of Public Health Sciences, University of Virginia, Charlottesville, VA, USA.ORCID 0000-0003-3099-6462
Mathew DevallCenter for Public Health Genomics, Department of Public Health Sciences, University of Virginia, Charlottesville, VA, USA.
Fredrick SchumacherDepartment of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA.ORCID 0000-0002-3073-7463
Marilena MelasThe Steve and Cindy Rasmussen Institute for Genomic Medicine, Nationwide Children's Hospital, Columbus, OH, USA.
Gad RennertDepartment of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.ORCID 0000-0002-8512-068X
Mireia Obón-SantacanaColorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute, Barcelona, Spain.
Vicente Martín-SánchezConsortium for Biomedical Research in Epidemiology and Public Health, Madrid, Madrid, Spain.
Ferran Moratalla-NavarroColorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute, Barcelona, Spain.
Jae Hwan OhCenter for Colorectal Cancer, National Cancer Center Hospital, National Cancer Center, Gyeonggi-do, South Korea.
Jeongseon KimDepartment of Cancer Biomedical Science, Graduate School of Cancer Science and Policy, National Cancer Center, Gyeonggi-do, South Korea.ORCID 0000-0002-0889-2686
Sun Ha JeeDepartment of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, South Korea.
Keum Ji JungDepartment of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, South Korea.
Sun-Seog KweonDepartment of Preventive Medicine, Chonnam National University Medical School, Gwangju, South Korea.
Min-Ho ShinDepartment of Preventive Medicine, Chonnam National University Medical School, Gwangju, South Korea.ORCID 0000-0002-2217-5624
Aesun ShinDepartment of Preventive Medicine, Seoul National University College of Medicine, Seoul, South Korea.
Yoon-Ok AhnDepartment of Preventive Medicine, Seoul National University College of Medicine, Seoul, South Korea.
Dong-Hyun KimDepartment of Social and Preventive Medicine, Hallym University College of Medicine, Okcheon-dong, South Korea.
Isao OzeDivision of Cancer Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan.ORCID 0000-0002-0762-1147
Wanqing WenDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA.ORCID 0000-0002-3004-5168
Keitaro MatsuoDivision of Molecular and Clinical Epidemiology, Aichi Cancer Center Research Institute, Nagoya, Japan.ORCID 0000-0003-1761-6314
Koichi MatsudaLaboratory of Clinical Genome Sequencing, Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan.ORCID 0000-0001-7292-2686
Chizu TanikawaLaboratory of Genome Technology, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
Zefang RenSchool of Public Health, Sun Yat-sen University, Guangzhou, China.ORCID 0000-0002-7785-4704
Yu-Tang GaoState Key Laboratory of Oncogenes and Related Genes and Department of Epidemiology, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China.
Wei-Hua JiaState Key Laboratory of Oncology in South China, Cancer Center, Sun Yat-sen University, Guangzhou, China.ORCID 0000-0002-0528-8715
John HopperCentre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.
Mark JenkinsCentre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.ORCID 0000-0002-8964-6160
Aung Ko WinCentre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.ORCID 0000-0002-2794-5261
Rish PaiDepartment of Laboratory Medicine and Pathology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
Jane FigueiredoDepartment of Preventive Medicine, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Robert HaileDivision of Oncology, Department of Medicine, Cedars-Sinai Cancer Research Center for Health Equity, Los Angeles, CA, USA.ORCID 0000-0001-6902-1836
Steven GallingerLunenfeld Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada.
Michael WoodsDivision of Biomedical Sciences, Memorial University of Newfoundland, St. John, Ontario, Canada.
Polly NewcombPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0001-8786-0043
David DugganCity of Hope National Medical Center, Translational Genomics Research Institute, Phoenix, AZ, USA.
Jeremy CheadleInstitute of Medical Genetics, Cardiff University, Cardiff, UK.ORCID 0000-0001-9453-8458
Richard KaplanMRC Clinical Trials Unit, Medical Research Council, Cardiff, UK.ORCID 0000-0002-0189-8348
Timothy MaughanMRC Institute for Radiation Oncology, University of Oxford, Oxford, UK.
Rachel KerrDepartment of Oncology, University of Oxford, Oxford, UK.
David KerrRadcliffe Department of Medicine, University of Oxford, Oxford, UK.ORCID 0000-0001-7811-6722
Iva KiracDepartment of Surgical Oncology, University Hospital for Tumors, Sestre milosrdnice University Hospital Center, Zagreb, Croatia.
Jan BöhmDepartment of Pathology, Central Finland Health Care District, Jyväskylä, Finland.
Lukka-Pekka MecklinCentral Finland Health Care District, Jyväskylä, Finland.
Pekka JousilahtiDepartment of Health and Welfare, Finnish Institute for Health and Welfare, Helsinki, Finland.ORCID 0000-0001-7190-0979
Paul KnektDepartment of Health and Welfare, Finnish Institute for Health and Welfare, Helsinki, Finland.
Lauri AaltonenDepartment of Medical and Clinical Genetics, University of Helsinki, Helsinki, Finland.ORCID 0000-0001-6839-4286
Harri RissanenDepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki, Finland.
Eero PukkalaFinnish Cancer Registry, Institute for Statistical and Epidemiological Cancer Research, Helsinki, Finland.
Johan ErikssonFolkhälsan Research Centre, University of Helsinki, Helsinki, Finland.
Tatiana CajusoDepartment of Medical and Clinical Genetics, University of Helsinki, Helsinki, Finland.ORCID 0000-0002-6354-5572
Ulrika HänninenDepartment of Medical and Clinical Genetics, University of Helsinki, Helsinki, Finland.
Johanna KondelinDepartment of Medical and Clinical Genetics, University of Helsinki, Helsinki, Finland.
Kimmo PalinDepartment of Medical and Clinical Genetics, University of Helsinki, Helsinki, Finland.ORCID 0000-0002-4621-6128
Tomas TanskanenDepartment of Medical and Clinical Genetics, University of Helsinki, Helsinki, Finland.
Laura Renkonen-SinisaloDepartment of Surgery, Abdominal Centre, Helsinki University Hospital, Helsinki, Finland.
Brent ZankeDepartment of Oncology, University of Toronto, Toronto, Ontario, Canada.
Satu MännistöDepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki, Finland.ORCID 0000-0002-8668-3046
Demetrius AlbanesDivision of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Stephanie WeinsteinDivision of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.ORCID 0000-0002-3834-1535
Edward Ruiz-NarvaezDepartment of Nutritional Sciences, School of Public Health, University of Michigan, Ann Arbor, MI, USA.ORCID 0000-0002-0339-5824
Julie PalmerSlone Epidemiology Center at Boston University, Boston, MA, USA.
Daniel BuchananColorectal Oncogenomics Group, Department of Clinical Pathology, University of Melbourne, Parkville, Victoria, Australia.ORCID 0000-0003-2225-6675
Elizabeth PlatzDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.ORCID 0000-0003-3676-8954
Kala VisvanathanDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.ORCID 0000-0002-0582-8005
Cornelia UlrichHuntsman Cancer Institute and Department of Population Health Sciences, University of Utah, Salt Lake City, UT, USA.
Erin SiegelCancer Epidemiology Program, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.ORCID 0000-0003-1779-2510
Stefanie BrezinaInstitute of Cancer Research, Department of Medicine I, Medical University Vienna, Vienna, Austria.ORCID 0000-0001-5238-6900
Andrea GsurInstitute of Cancer Research, Department of Medicine I, Medical University Vienna, Vienna, Austria.ORCID 0000-0002-9795-1528
Peter CampbellDepartment of Epidemiology and Population Health, Albert Einstein College of Medicine, New York, NY, USA.
Jenny Chang-ClaudeDivision of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.ORCID 0000-0001-8919-1971
Michael HoffmeisterDivision of Clinical Epidemiology and Aging Research, German Cancer Research Center, Heidelberg, Germany.ORCID 0000-0002-8307-3197
Hermann BrennerDivision of Clinical Epidemiology and Aging Research, German Cancer Research Center, Heidelberg, Germany.
Martha SlatteryDepartment of Internal Medicine, University of Utah, Salt Lake City, UT, USA.
John PotterPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0001-5439-1500
Konstantinos TsilidisDepartment of Hygiene and Epidemiology, University of Ioannina School of Medicine, Ioannina, Greece.ORCID 0000-0002-8452-8472
Matthias SchulzeDepartment of Molecular Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal, Germany.ORCID 0000-0002-0830-5277
Marc GunterNutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.
Neil MurphyNutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France.ORCID 0000-0003-3347-8249
Antoni CastellsGastroenterology Department, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, University of Barcelona, Barcelona, Spain.
Sergi Castellví-BelGastroenterology Department, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, University of Barcelona, Barcelona, Spain.ORCID 0000-0003-1217-5097
Leticia MoreiraGastroenterology Department, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, University of Barcelona, Barcelona, Spain.ORCID 0000-0002-4518-8591
Volker ArndtDivision of Clinical Epidemiology and Aging Research, German Cancer Research Center, Heidelberg, Germany.ORCID 0000-0001-9320-8684
Anna ShcherbinaDepartment of Genetics, Stanford University, Stanford, CA, USA.
Mariana SternDepartment of Population and Public Health Sciences, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Bens PardameanBioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
Timothy BishopLeeds Institute of Medical Research at St James's, University of Leeds, Leeds, UK.ORCID 0000-0002-8752-8785
Graham GilesCentre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.ORCID 0000-0003-4946-9099
Melissa SoutheyCancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.ORCID 0000-0002-6313-9005
Gregory IdosDepartment of Medical Oncology and Center For Precision Medicine, City of Hope National Medical Center, Duarte, CA, USA.
Kevin McDonnellRuth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel.
Zomoroda Abu-FulDepartment of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.
Joel GreensonRuth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel.
Katerina ShulmanDepartment of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.
Flavio LejbkowiczDepartment of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.
Kenneth OffitClinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
Yu-Ru SuKaiser Permanente Washington Health Research Institute, Seattle, WA, USA.
Robert SteinfelderPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Temitope KekuCenter for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC, USA.
Bethany van GuelpenDepartment of Radiation Sciences, Oncology Unit, Umeå University, Umeå, Sweden.ORCID 0000-0002-9692-101X
Thomas HudsonOntario Institute for Cancer Research, Toronto, Ontario, Canada.ORCID 0000-0002-1376-4849
Heather HampelDivision of Human Genetics, Department of Internal Medicine, Ohio State University Comprehensive Cancer Center, Columbus, OH, USA.ORCID 0000-0001-7558-9794
Rachel PearlmanDivision of Human Genetics, Department of Internal Medicine, Ohio State University Comprehensive Cancer Center, Columbus, OH, USA.
Sonja BerndtDivision of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Richard HayesDivision of Epidemiology, Department of Population Health, New York University School of Medicine, New York, NY, USA.ORCID 0000-0002-0918-661X
Marie Elena MartinezPopulation Sciences, Disparities and Community Engagement, University of California San Diego Moores Cancer Center, La Jolla, CA, USA.
Sushma ThomasFred Hutchinson Cancer Research Center, Seattle, WA, USA.
Douglas CorleyDivision of Research, Kaiser Permanente Northern California, Oakland, CA, USA.
Paul PharoahDepartment of Public Health and Primary Care, University of Cambridge, Cambridge, UK.ORCID 0000-0001-8494-732X
Susanna LarssonInstitute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.ORCID 0000-0003-0118-0341
Yun YenTaipei Medical University, Taipei, Taiwan.ORCID 0000-0003-0815-412X
Heinz-Josef LenzDepartment of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.ORCID 0000-0003-2178-9568
Emily WhitePublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Li LiCase Comprehensive Cancer Center, Case Western Reserve University, Cleveland, OH, USA.
Kimberly DohenyCenter for Inherited Disease Research, Department of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.ORCID 0000-0001-8806-5738
Elizabeth PughCenter for Inherited Disease Research, Department of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Tameka ShelfordCenter for Inherited Disease Research, Department of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Andrew ChanClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.ORCID 0000-0001-7284-6767
Marcia Cruz-CorreaComprehensive Cancer Center, University of Puerto Rico, San Juan, Puerto Rico.
Annika LindblomDepartment of Clinical Genetics, Karolinska University Hospital, Stockholm, Sweden.
David HunterDepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
Amit JoshiClinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.ORCID 0000-0001-7581-6934
Clemens SchafmayerDepartment of General Surgery, University Hospital Rostock, Rostock, Germany.
Peter ScacheriDepartment of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, OH, USA.
Anshul KundajeDepartment of Genetics, Stanford University, Stanford, CA, USA.ORCID 0000-0003-3084-2287
Deborah NickersonDepartment of Genome Sciences, University of Washington, Seattle, WA, USA.
Robert SchoenDepartment of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.ORCID 0000-0001-7153-2766
Jochen HampeDepartment of Medicine I, University Hospital Dresden, Technische Universität Dresden, Dresden, Germany.ORCID 0000-0002-2421-6127
Zsofia StadlerDepartment of Medicine, Weill Cornell Medical College, New York, NY, USA.
Pavel VodickaDepartment of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
Ludmila VodickovaDepartment of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
Veronika VymetalkovaDepartment of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
Nickolas PapadopoulosDepartment of Oncology Ludwig Center at the Sidney Kimmel Cancer Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA.ORCID 0000-0001-7135-7451
Chistopher EdlundDepartment of Preventive Medicine, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
William GaudermanDepartment of Preventive Medicine, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Duncan ThomasDepartment of Preventive Medicine, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.ORCID 0000-0002-6040-8804
David ShibataDepartment of Surgery, University of Tennessee Health Science Center, Memphis, TN, USA.
Amanda TolandDepartments of Cancer Biology and Genetics and Internal Medicine, Comprehensive Cancer Center, Ohio State University, Columbus, OH, USA.ORCID 0000-0002-0271-1792
Sanford MarkowitzDepartments of Medicine and Genetics, Case Comprehensive Cancer Center, Case Western Reserve University and University Hospitals of Cleveland, Cleveland, OH, USA.
Andre KimDepartment of Preventive Medicine, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Stephen ChanockDivision of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.ORCID 0000-0002-2324-3393
Franzel van DuijnhovenDivision of Human Nutrition and Health, Wageningen University and Research, Wageningen, The Netherlands.
Edith FeskensDivision of Human Nutrition, Wageningen University and Research, Wageningen, The Netherlands.ORCID 0000-0001-5819-2488
Lori SakodaPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0002-0900-5735
Manuela Gago-DominguezGenomic Medicine Group, Galician Public Foundation of Genomic Medicine, Servicio Galego de Saude, Santiago de Compostela, Spain.
Alicja WolkInstitute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.ORCID 0000-0001-7387-6845
Alessio NaccaratiItalian Institute for Genomic Medicine, Candiolo Cancer Institute FPO-IRCCS, Candiolo (TO), Italy.ORCID 0000-0001-5774-0905
Barbara PardiniItalian Institute for Genomic Medicine, Candiolo Cancer Institute FPO-IRCCS, Candiolo (TO), Italy.ORCID 0000-0001-9571-4257
Liesel FitzGeraldCancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.ORCID 0000-0002-6882-2698
Soo Chin LeeNational University Cancer Institute, Singapore, Cancer Science Institute of Singapore, National University of Singapore, Singapore, Singapore.
Shuji OginoDepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.ORCID 0000-0002-3909-2323
Stephanie BienPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Charles KooperbergPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.ORCID 0000-0002-7986-8560
Christopher LiPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Yi LinPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Ross PrenticePublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Conghui QuPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Stéphane BézieauService de Génétique Médicale, Centre Hospitalier Universitaire Nantes, Nantes, France.ORCID 0000-0003-0095-1319
Catherine TangenSWOG Statistical Center, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Elaine MardisDepartment of Pediatrics, Nationwide Children's Hospital, The Steve and Cindy Rasmussen Institute for Genomic Medicine, Columbus, OH, USA.ORCID 0000-0002-5892-1553
Taiki YamajiDivision of Epidemiology, National Cancer Center Institute for Cancer Control, National Cancer Center, Tokyo, Japan.
Norie SawadaDivision of Cohort Research, National Cancer Center Institute for Cancer Control, National Cancer Center, Tokyo, Japan.ORCID 0000-0002-9936-1476
Motoki IwasakiDivision of Epidemiology, National Cancer Center Institute for Cancer Control, National Cancer Center, Tokyo, Japan.
Christopher HaimanDepartment of Preventive Medicine, Center for Genetic Epidemiology, University of Southern California, Los Angeles, CA, USA.ORCID 0000-0002-0097-9971
Loic Le MarchandCancer Center, University of Hawaii, Honolulu, HI, USA.
Anna WuPreventative Medicine, University of Southern California, Los Angeles, CA, USA.
Chenxu QuUSC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Caroline McNeilUSC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Gerhard CoetzeeVan Andel Research Institute, Grand Rapids, MI, USA.ORCID 0000-0001-8820-8364
Caroline HaywardMRC Human Genetics Unit, Institute of Genomics and Cancer, University of Edinburgh, Edinburgh, UK.ORCID 0000-0002-9405-9550
Ian DearyLothian Birth Cohorts group, Department of Psychology, University of Edinburgh, Edinburgh, UK.ORCID 0000-0002-1733-263X
Sarah HarrisLothian Birth Cohorts group, Department of Psychology, University of Edinburgh, Edinburgh, UK.ORCID 0000-0002-4941-5106
Evropi TheodoratouCentre for Global Health, Usher Institute, University of Edinburgh, Edinburgh, UK.
Stuart ReidColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.
Marion WalkerColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.
Li Yin OoiColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.ORCID 0000-0002-5588-2130
Victor MorenoColorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute, Barcelona, Spain.ORCID 0000-0002-2818-5487
Graham CaseyCenter for Public Health Genomics, Department of Public Health Sciences, University of Virginia, Charlottesville, VA, USA.
Stephen GruberDepartment of Medical Oncology and Center For Precision Medicine, City of Hope National Medical Center, Duarte, CA, USA.
Ian TomlinsonEdinburgh Cancer Research Centre, Institute of Genomics and Cancer, University of Edinburgh, Edinburgh, UK. Ian.Tomlinson@ed.ac.uk.ORCID 0000-0003-3037-1470
Wei ZhengDivision of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt Epidemiology Center, Vanderbilt University Medical Center, Nashville, TN, USA. wei.zheng@vanderbilt.edu.ORCID 0000-0003-1226-070X
Malcolm DunlopColon Cancer Genetics Group, Medical Research Council Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK. malcolm.dunlop@ed.ac.uk.ORCID 0000-0002-3033-5851
Richard HoulstonDivision of Genetics and Epidemiology, Institute of Cancer Research, London, UK. Richard.Houlston@icr.ac.uk.ORCID 0000-0002-5268-0242
Ulrike PetersPublic Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA. upeters@fredhutch.org.ORCID 0000-0001-5666-9318
University of Southern California · USFred Hutch Cancer Center · USInstitute of Genetics and Cancer · GBUniversity of Helsinki · FIVanderbilt University Medical Center · USJohns Hopkins University · USUniversity of Washington · USEdinburgh Cancer Research · GBThe University of Melbourne · AUFinnish Institute for Health and Welfare · FIInstitut d'Investigació Biomédica de Bellvitge · ESInstitute of Cancer Research · GBNational Institutes of Health · USUniversity of Oxford · GBCarmel Medical Center · ILCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas · ESCharles University · CZCity Of Hope National Medical Center · USGerman Cancer Research Center · DEUniversity of Virginia · US

Funding

X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI SELWYN M VICKERS · 1985 to 2026
$347.4M
Translational Bioimaging Core Shared ResourceP30CA015704 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI Eric Collisson · 1985 to 2026
$296.4M
USC/NORRIS COMPREHENSIVE CANCER CENTER (CORE) SUPPORTP30CA014089 · NCI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI Fumito Ito · 1985 to 2026
$181.4M
Tumor Immunology and Microenvironment Research ProgramP30CA068485 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI Ben Ho Park · 1995 to 2026
$172.8M
Translational Therapeutics Research Program (TT)P30CA016058 · NCI · OHIO STATE UNIVERSITY · PI Daniel G. Stover · 1985 to 2026
$132.3M
UNC-CH CENTER FOR ENVIRONMENTAL HEALTH &SUSCEPTIBILITYP30ES010126 · NIEHS · UNIV OF NORTH CAROLINA CHAPEL HILL · PI Hazel B Nichols · 2001 to 2026
$36.3M
Statistical Methods for Integrative Genomics in CancerP01CA196569 · NCI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI David V Conti · 2016 to 2026
$25.5M
Alpha-Tocopherol, Beta-Carotene Cancer Prevention (ATBC) StudyZIACP010195 · NCI · DIVISION OF CANCER EPIDEMIOLOGY AND GENETICS · PI ALBANES, DEMETRIUS · 2009 to 2025
$22.5M
Molecular pathological epidemiology of colorectal cancerU01CA137088 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI PETERS, ULRIKE · 2009 to 2018
$21.8M
Data sharing: the Colon Cancer Family Registry CohortU01CA167551 · NCI · UNIVERSITY OF MELBOURNE · PI Daniel David BUCHANAN, Steven Gallinger · 2018 to 2026
$16.8M
ONTARIO REGISTRY FOR STUDIES OF FAMILIAL COLON CANCERU01CA074783 · NCI · CANCER CARE ONTARIO · PI GALLINGER, STEVEN · 1997 to 2008
$12.5M
Detection of Colorectal Cancer Susceptibility Loci Using Genome-Wide SequencingU01CA164930 · NCI · FRED HUTCHINSON CANCER RESEARCH CENTER · PI PETERS, ULRIKE · 2012 to 2015
$12.4M
Cancer Research UK 12076Cancer Research UK 18927Cancer Research UK 19167Cancer Research UK 22804Cancer Research UK 25514Cancer Research UK 27327Cancer Research UK 29186Cancer Research UK C1298/A25514Cancer Research UK C348/A12076Cancer Research UK C6199/A16459Cancer Research UK C6199/A27327Medical Research Council G0700704Medical Research Council MC_PC_U127527198Medical Research Council MC_U127527198Medical Research Council MC_UU_00007/1Medical Research Council MC_UU_00007/10Medical Research Council MR/K018647/1Medical Research Council MR/K026992/1Medical Research Council MR/P001106/1NCI NIH HHS P01 CA196569NCI NIH HHS P30 CA008748NCI NIH HHS P30 CA014089NCI NIH HHS P30 CA015704NCI NIH HHS P30 CA016058NCI NIH HHS P30 CA068485NCI NIH HHS R01 CA059045NCI NIH HHS R01 CA081488NCI NIH HHS R01 CA124558NCI NIH HHS R01 CA148667NCI NIH HHS R01 CA158473NCI NIH HHS R01 CA188214NCI NIH HHS R01 CA197350NCI NIH HHS R01 CA201407NCI NIH HHS R01 CA206279NCI NIH HHS R01 CA244588NCI NIH HHS R01 CA269589NCI NIH HHS R35 CA197442NCI NIH HHS R37 CA070867NCI NIH HHS R37 CA227130NCI NIH HHS U01 CA074783NCI NIH HHS U01 CA137088NCI NIH HHS U01 CA164930NCI NIH HHS U01 CA167551NCI NIH HHS U19 CA148107NCI NIH HHS UM1 CA182910NHLBI NIH HHS HHSN268201200008CNHLBI NIH HHS HHSN268201200008INIEHS NIH HHS P30 ES010126NIEHS NIH HHS T32 ES013678NIH HHS S10 OD028685World Health Organization 001
6 · The paper itself

Abstract

Colorectal cancer (CRC) is a leading cause of mortality worldwide. We conducted a genome-wide association study meta-analysis of 100,204 CRC cases and 154,587 controls of European and east Asian ancestry, identifying 205 independent risk associations, of which 50 were unreported. We performed integrative genomic, transcriptomic and methylomic analyses across large bowel mucosa and other tissues. Transcriptome- and methylome-wide association studies revealed an additional 53 risk associations. We identified 155 high-confidence effector genes functionally linked to CRC risk, many of which had no previously established role in CRC. These have multiple different functions and specifically indicate that variation in normal colorectal homeostasis, proliferation, cell adhesion, migration, immunity and microbial interactions determines CRC risk. Crosstissue analyses indicated that over a third of effector genes most probably act outside the colonic mucosa. Our findings provide insights into colorectal oncogenesis and highlight potential targets across tissues for new CRC treatment and chemoprevention strategies.

Indexed as

Colorectal NeoplasmsEast Asian PeopleEuropean PeopleGenetic Predisposition to DiseaseGenome-Wide Association StudyHumansMultiomicsPolymorphism, Single Nucleotide

Identifiers

PMID36539618
PMCPMC10094749
OpenAlexW4312066528

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