. 2025 Jan 1;36(1):126-138.

doi: 10.1097/EDE.0000000000001795. Epub 2024 Sep 24.

Characterization of Additive Gene-environment Interactions For Colorectal Cancer Risk

Claire E Thomas¹, Yi Lin¹, Michelle Kim¹, Eric S Kawaguchi², Conghui Qu¹, Caroline Y Um³, Brigid M Lynch^{4

5}, Bethany Van Guelpen^{6

7}, Kostas Tsilidis^{8

9}, Robert Carreras-Torres^{10

11}, Franzel J B van Duijnhoven¹², Lori C Sakoda^{1

13}, Peter T Campbell¹⁴, Yu Tian^{15

16}, Jenny Chang-Claude^{15

17}, Stéphane Bézieau¹⁸, Arif Budiarto^{19

20}, Julie R Palmer²¹, Polly A Newcomb^{1

22}, Graham Casey²³, Loic Le Marchandz²⁴, Marios Giannakis^{25

26

27}, Christopher I Li¹, Andrea Gsur²⁸, Christina Newton³, Mireia Obón-Santacana^{29

30

31}, Victor Moreno^{29

30

31

32}, Pavel Vodicka^{33

34

35}, Hermann Brenner^{36

37

38}, Michael Hoffmeister³⁶, Andrew J Pellatt³⁹, Robert E Schoen⁴⁰, Niki Dimou⁴¹, Neil Murphy⁴¹, Marc J Gunter⁴¹, Sergi Castellví-Bel⁴², Jane C Figueiredo^{43

44}, Andrew T Chan^{45

46

47

48

49

50}, Mingyang Song^{47

51

52}, Li Li⁵³, D Timothy Bishop⁵⁴, Stephen B Gruber⁵⁵, James W Baurley^{19

56}, Stephanie A Bien¹, David V Conti², Jeroen R Huyghe¹, Anshul Kundaje^{57

58}, Yu-Ru Su¹, Jun Wang^{59

60}, Temitope O Keku⁶¹, Michael O Woods⁶², Sonja I Berndt⁶³, Stephen J Chanock⁶³, Catherine M Tangen⁶⁴, Alicja Wolk⁶⁵, Andrea Burnett-Hartman⁶⁶, Anna H Wu⁶⁷, Emily White^{1

68}, Matthew A Devall⁵³, Virginia Díez-Obrero⁶⁹, David A Drew⁷⁰, Edward Giovannucci^{71

72}, Akihisa Hidaka¹, Andre E Kim², Juan Pablo Lewinger², John Morrison², Jennifer Ose^{73

74}, Nikos Papadimitriou⁴¹, Bens Pardamean¹⁹, Anita R Peoples^{73

74}, Edward A Ruiz-Narvaez⁷⁵, Anna Shcherbina^{57

58}, Mariana C Stern⁴⁴, Xuechen Chen³⁶, Duncan C Thomas², Elizabeth A Platz⁷⁶, W James Gauderman², Ulrike Peters^{1

22}, Li Hsu^{1

72}

Affiliations

¹ From the Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA.
² Division of Biostatistics, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA.
³ Department of Population Science, American Cancer Society, Atlanta, GA.
⁴ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
⁵ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Victoria, Australia.
⁶ Department of Radiation Sciences, Oncology Unit, Umeå University, Umeå, Sweden.
⁷ Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Sweden.
⁸ Department of Epidemiology and Biostatistics, Imperial College London, School of Public Health, London, UK.
⁹ Department of Hygiene and Epidemiology, University of Ioannina, School of Medicine, Ioannina, Greece.
¹⁰ Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
¹¹ Digestive Diseases and Microbiota Group, Girona Biomedical Research Institute (IDIBGI), Salt, Girona, Spain.
¹² Division of Human Nutrition and Health, Wageningen University & Research, Wageningen, The Netherlands.
¹³ Division of Research, Kaiser Permanente Northern California, Oakland, CA.
¹⁴ Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY.
¹⁵ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁶ School of Public Health, Capital Medical University, Beijing, China.
¹⁷ University Medical Centre Hamburg-Eppendorf, University Cancer Centre Hamburg (UCCH), Hamburg, Germany.
¹⁸ Service de Génétique Médicale, Centre Hospitalier Universitaire (CHU) Nantes, Nantes, France.
¹⁹ Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
²⁰ Computer Science Department, School of Computer Science, Bina Nusantara University, Jakarta, Indonesia.
²¹ Slone Epidemiology Center at Boston University, Boston, MA.
²² Department of Epidemiology, University of Washington, Seattle, WA.
²³ Center for Public Health Genomics, University of Virginia, Charlottesville, VA.
²⁴ University of Hawaii Cancer Center, Honolulu, HI.
²⁵ Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA.
²⁶ Broad Institute of MIT and Harvard, Cambridge, MA.
²⁷ Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA.
²⁸ Center for Cancer Research, Medical University of Vienna, Vienna, Austria.
²⁹ Unit of Biomarkers and Suceptibility (UBS), Oncology Data Analytics Program (ODAP), Catalan Institute of Oncology (ICO), L'Hospitalet del Llobregat, Barcelona, Spain.
³⁰ ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
³¹ Consortium for Biomedical Research in Epidemiology and Public Health (CIBERESP), Madrid, Spain.
³² Department of Clinical Sciences, Faculty of Medicine and health Sciences and Universitat de Barcelona Institute of Complex Systems (UBICS), University of Barcelona (UB), L'Hospitalet de Llobregat, Barcelona, Spain.
³³ Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
³⁴ Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.
³⁵ Faculty of Medicine and Biomedical Center in Pilsen, Charles University, Pilsen, Czech Republic.
³⁶ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁷ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³⁸ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁹ Department of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX.
⁴⁰ Departments of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, PA.
⁴¹ Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France.
⁴² Gastroenterology Department, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), University of Barcelona, Barcelona, Spain.
⁴³ Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA.
⁴⁴ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA.
⁴⁵ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
⁴⁶ Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
⁴⁷ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
⁴⁸ Broad Institute of Harvard and MIT, Cambridge, MA.
⁴⁹ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA.
⁵⁰ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA.
⁵¹ Departments of Epidemiology and Nutrition, Harvard TH Chan School of Public Health, Boston, MA.
⁵² Department of Nutrition, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA.
⁵³ Department of Family Medicine, University of Virginia, Charlottesville, VA.
⁵⁴ Leeds Institute of Medical Research, University of Leeds, Leeds, UK.
⁵⁵ Department of Medical Oncology & Therapeutics Research, City of Hope National Medical Center, Duarte CA.
⁵⁶ BioRealm LLC, Walnut, CA.
⁵⁷ Department of Genetics, Stanford University, Stanford, CA.
⁵⁸ Department of Computer Science, Stanford University, Stanford, CA.
⁵⁹ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA.
⁶⁰ Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA.
⁶¹ Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC.
⁶² Memorial University of Newfoundland, Discipline of Genetics, St. John's, Canada.
⁶³ Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD.
⁶⁴ SWOG Statistical Center, Fred Hutchinson Cancer Center, Seattle, WA.
⁶⁵ Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁶⁶ Institute for Health Research, Kaiser Permanente Colorado, Aurora, CO.
⁶⁷ University of Southern California, Department of Population and Public Health Sciences, Los Angeles, CA.
⁶⁸ Department of Epidemiology, University of Washington School of Public Health, Seattle, WA.
⁶⁹ Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark.
⁷⁰ Clinical & Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
⁷¹ Harvard TH Chan School of Public Health.
⁷² Department of Biostatistics, University of Washington, Seattle, WA.
⁷³ Huntsman Cancer Institute, Salt Lake City, UT.
⁷⁴ Department of Population Health Sciences, University of Utah, Salt Lake City, UT.
⁷⁵ Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI.
⁷⁶ Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD.

PMID: 39316822
PMCID: PMC12142706 (available on 2026-01-01)
DOI: 10.1097/EDE.0000000000001795

Characterization of Additive Gene-environment Interactions For Colorectal Cancer Risk

Claire E Thomas et al. Epidemiology. 2025.

. 2025 Jan 1;36(1):126-138.

doi: 10.1097/EDE.0000000000001795. Epub 2024 Sep 24.

Authors

Affiliations

¹ From the Public Health Sciences Division, Fred Hutchinson Cancer Center, Seattle, WA.
² Division of Biostatistics, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA.
³ Department of Population Science, American Cancer Society, Atlanta, GA.
⁴ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
⁵ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Victoria, Australia.
⁶ Department of Radiation Sciences, Oncology Unit, Umeå University, Umeå, Sweden.
⁷ Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Sweden.
⁸ Department of Epidemiology and Biostatistics, Imperial College London, School of Public Health, London, UK.
⁹ Department of Hygiene and Epidemiology, University of Ioannina, School of Medicine, Ioannina, Greece.
¹⁰ Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
¹¹ Digestive Diseases and Microbiota Group, Girona Biomedical Research Institute (IDIBGI), Salt, Girona, Spain.
¹² Division of Human Nutrition and Health, Wageningen University & Research, Wageningen, The Netherlands.
¹³ Division of Research, Kaiser Permanente Northern California, Oakland, CA.
¹⁴ Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY.
¹⁵ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁶ School of Public Health, Capital Medical University, Beijing, China.
¹⁷ University Medical Centre Hamburg-Eppendorf, University Cancer Centre Hamburg (UCCH), Hamburg, Germany.
¹⁸ Service de Génétique Médicale, Centre Hospitalier Universitaire (CHU) Nantes, Nantes, France.
¹⁹ Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
²⁰ Computer Science Department, School of Computer Science, Bina Nusantara University, Jakarta, Indonesia.
²¹ Slone Epidemiology Center at Boston University, Boston, MA.
²² Department of Epidemiology, University of Washington, Seattle, WA.
²³ Center for Public Health Genomics, University of Virginia, Charlottesville, VA.
²⁴ University of Hawaii Cancer Center, Honolulu, HI.
²⁵ Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA.
²⁶ Broad Institute of MIT and Harvard, Cambridge, MA.
²⁷ Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA.
²⁸ Center for Cancer Research, Medical University of Vienna, Vienna, Austria.
²⁹ Unit of Biomarkers and Suceptibility (UBS), Oncology Data Analytics Program (ODAP), Catalan Institute of Oncology (ICO), L'Hospitalet del Llobregat, Barcelona, Spain.
³⁰ ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
³¹ Consortium for Biomedical Research in Epidemiology and Public Health (CIBERESP), Madrid, Spain.
³² Department of Clinical Sciences, Faculty of Medicine and health Sciences and Universitat de Barcelona Institute of Complex Systems (UBICS), University of Barcelona (UB), L'Hospitalet de Llobregat, Barcelona, Spain.
³³ Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
³⁴ Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.
³⁵ Faculty of Medicine and Biomedical Center in Pilsen, Charles University, Pilsen, Czech Republic.
³⁶ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁷ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³⁸ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁹ Department of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX.
⁴⁰ Departments of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, PA.
⁴¹ Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France.
⁴² Gastroenterology Department, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), University of Barcelona, Barcelona, Spain.
⁴³ Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA.
⁴⁴ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA.
⁴⁵ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
⁴⁶ Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
⁴⁷ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
⁴⁸ Broad Institute of Harvard and MIT, Cambridge, MA.
⁴⁹ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA.
⁵⁰ Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA.
⁵¹ Departments of Epidemiology and Nutrition, Harvard TH Chan School of Public Health, Boston, MA.
⁵² Department of Nutrition, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA.
⁵³ Department of Family Medicine, University of Virginia, Charlottesville, VA.
⁵⁴ Leeds Institute of Medical Research, University of Leeds, Leeds, UK.
⁵⁵ Department of Medical Oncology & Therapeutics Research, City of Hope National Medical Center, Duarte CA.
⁵⁶ BioRealm LLC, Walnut, CA.
⁵⁷ Department of Genetics, Stanford University, Stanford, CA.
⁵⁸ Department of Computer Science, Stanford University, Stanford, CA.
⁵⁹ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA.
⁶⁰ Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA.
⁶¹ Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC.
⁶² Memorial University of Newfoundland, Discipline of Genetics, St. John's, Canada.
⁶³ Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD.
⁶⁴ SWOG Statistical Center, Fred Hutchinson Cancer Center, Seattle, WA.
⁶⁵ Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁶⁶ Institute for Health Research, Kaiser Permanente Colorado, Aurora, CO.
⁶⁷ University of Southern California, Department of Population and Public Health Sciences, Los Angeles, CA.
⁶⁸ Department of Epidemiology, University of Washington School of Public Health, Seattle, WA.
⁶⁹ Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark.
⁷⁰ Clinical & Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, MA.
⁷¹ Harvard TH Chan School of Public Health.
⁷² Department of Biostatistics, University of Washington, Seattle, WA.
⁷³ Huntsman Cancer Institute, Salt Lake City, UT.
⁷⁴ Department of Population Health Sciences, University of Utah, Salt Lake City, UT.
⁷⁵ Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, MI.
⁷⁶ Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD.

PMID: 39316822
PMCID: PMC12142706 (available on 2026-01-01)
DOI: 10.1097/EDE.0000000000001795

Abstract

Background: Colorectal cancer (CRC) is a common, fatal cancer. Identifying subgroups who may benefit more from intervention is of critical public health importance. Previous studies have assessed multiplicative interaction between genetic risk scores and environmental factors, but few have assessed additive interaction, the relevant public health measure.

Methods: Using resources from CRC consortia, including 45,247 CRC cases and 52,671 controls, we assessed multiplicative and additive interaction (relative excess risk due to interaction, RERI) using logistic regression between 13 harmonized environmental factors and genetic risk score, including 141 variants associated with CRC risk.

Results: There was no evidence of multiplicative interaction between environmental factors and genetic risk score. There was additive interaction where, for individuals with high genetic susceptibility, either heavy drinking (RERI = 0.24, 95% confidence interval [CI] = 0.13, 0.36), ever smoking (0.11 [0.05, 0.16]), high body mass index (female 0.09 [0.05, 0.13], male 0.10 [0.05, 0.14]), or high red meat intake (highest versus lowest quartile 0.18 [0.09, 0.27]) was associated with excess CRC risk greater than that for individuals with average genetic susceptibility. Conversely, we estimate those with high genetic susceptibility may benefit more from reducing CRC risk with aspirin/nonsteroidal anti-inflammatory drugs use (-0.16 [-0.20, -0.11]) or higher intake of fruit, fiber, or calcium (highest quartile versus lowest quartile -0.12 [-0.18, -0.050]; -0.16 [-0.23, -0.09]; -0.11 [-0.18, -0.05], respectively) than those with average genetic susceptibility.

Conclusions: Additive interaction is important to assess for identifying subgroups who may benefit from intervention. The subgroups identified in this study may help inform precision CRC prevention.

PubMed Disclaimer

Conflict of interest statement

S.G.: Brogent International LLC, co-founder, not related to submitted work. J.B.: co-founder and employee of BioRealm LLC. BioRealm LLC offers data analysis services, unrelated to this study. M.G.: Research funding from Servier and Janssen, unrelated to this study. Other authors report no conflicts of interest.

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Characterization of Additive Gene-environment Interactions For Colorectal Cancer Risk

Affiliations

Characterization of Additive Gene-environment Interactions For Colorectal Cancer Risk

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