Stephanie L Schmit1,2, Christopher K Edlund2, Fredrick R Schumacher3, Jian Gong4, Tabitha A Harrison4, Jeroen R Huyghe4, Chenxu Qu2,4, Marilena Melas2, David J Van Den Berg2, Hansong Wang5, Stephanie Tring2,6,7, Sarah J Plummer8, Demetrius Albanes9, M Henar Alonso10,11,12, Christopher I Amos13, Kristen Anton13, Aaron K Aragaki4, Volker Arndt14, Elizabeth L Barry15, Sonja I Berndt9, Stéphane Bezieau4, Stephanie Bien16, Amanda Bloomer1, Juergen Boehm17, Marie-Christine Boutron-Ruault18,19, Hermann Brenner14,20,21, Stefanie Brezina22, Daniel D Buchanan23,24,25, Katja Butterbach14, Bette J Caan26, Peter T Campbell27, Christopher S Carlson4, Jose E Castelao28, Andrew T Chan29,30, Jenny Chang-Claude31,32,33, Stephen J Chanock9, Iona Cheng34, Ya-Wen Cheng35, Lee Soo Chin36, James M Church37, Timothy Church38, Gerhard A Coetzee39, Michelle Cotterchio40, Marcia Cruz Correa41, Keith R Curtis4, David Duggan42, Douglas F Easton43, Dallas English44, Edith J M Feskens45, Rocky Fischer46, Liesel M FitzGerald44,47, Barbara K Fortini48, Lars G Fritsche49,50, Charles S Fuchs51,52, Manuela Gago-Dominguez53,54, Manish Gala29, Steven J Gallinger55, W James Gauderman2, Graham G Giles23,44, Edward L Giovannucci32,56, Stephanie M Gogarten57, Clicerio Gonzalez-Villalpando58, Elena M Gonzalez-Villalpando59, William M Grady60, Joel K Greenson61, Andrea Gsur62, Marc Gunter30, Christopher A Haiman2, Jochen Hampe63, Sophia Harlid64, John F Harju46, Richard B Hayes65, Philipp Hofer62, Michael Hoffmeister14, John L Hopper66, Shu-Chen Huang2, Jose Maria Huerta67, Thomas J Hudson68,69, David J Hunter70, Gregory E Idos2, Motoki Iwasaki71, Rebecca D Jackson72, Eric J Jacobs27, Sun Ha Jee73, Mark A Jenkins23, Wei-Hua Jia74, Shuo Jiao4, Amit D Joshi30,70, Laurence N Kolonel75, Suminori Kono22, Charles Kooperberg4, Vittorio Krogh76, Tilman Kuehn77, Sébastien Küry78, Andrea LaCroix4, Cecelia A Laurie57, Flavio Lejbkowicz1, Mathieu Lemire69, Heinz-Josef Lenz2,79, David Levine57, Christopher I Li80, Li Li81, Wolfgang Lieb82, Yi Lin4, Noralane M Lindor83, Yun-Ru Liu84, Fotios Loupakis35, Yingchang Lu85, Frank Luh86, Jing Ma87, Christoph Mancao88, Frank J Manion46, Sanford D Markowitz89, Vicente Martin90, Koichi Matsuda91, Keitaro Matsuo92,93, Kevin J McDonnell2, Caroline E McNeil2, Roger Milne23,44, Antonio J Molina11,94, Bhramar Mukherjee46, Neil Murphy95, Polly A Newcomb4, Kenneth Offit96, Hanane Omichessan18,19, Domenico Palli97, Jesus P Paredes Cotoré98, Julyann Pérez-Mayoral99, Paul D Pharoah100, John D Potter4, Conghui Qu2,4, Leon Raskin85,91, Gad Rennert86,101,102, Hedy S Rennert86,101, Bridget M Riggs1, Clemens Schafmayer103, Robert E Schoen104, Thomas A Sellers1, Daniela Seminara105, Gianluca Severi18,106, Wei Shi107, David Shibata108, Xiao-Ou Shu85,91, Erin M Siegel1, Martha L Slattery109, Melissa Southey24, Zsofia K Stadler96,110, Mariana C Stern2, Sebastian Stintzing111, Darin Taverna112, Stephen N Thibodeau113, Duncan C Thomas2, Antonia Trichopoulou114, Shoichiro Tsugane2,6,7, Cornelia M Ulrich17, Franzel J B van Duijnhoven45, Bethany van Guelpan, Joseph Vijai96, Jarmo Virtamo115, Stephanie J Weinstein9, Emily White4, Aung Ko Win23, Alicja Wolk116, Michael Woods117, Anna H Wu2, Kana Wu118, Yong-Bing Xiang119, Yun Yen35,120, Brent W Zanke121,122, Yi-Xin Zeng74, Ben Zhang123, Niha Zubair4, Sun-Seog Kweon124,125, Jane C Figueiredo126,127, Wei Zheng85,91, Loic Le Marchand5, Annika Lindblom128, Victor Moreno10,11,12, Ulrike Peters129, Graham Casey8, Li Hsu4, David V Conti2, Stephen B Gruber2,79. 1. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL. 2. Department of Preventive Medicine, USC Norris Comprehensive Cancer Center. 3. Department of Epidemiology and Biostatistics. 4. Public Health Sciences Division. 5. Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI. 6. National Cancer Center, Tokyo, Japan. 7. Center for Public Health Sciences, National Cancer Center, Tokyo, Japan. 8. Center for Public Health Genomics, University of Virginia, Charlottesville, VA. 9. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD. 10. Catalan Institute of Oncology, Bellvitge Biomedical Research Institute. 11. CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain. 12. University of Barcelona, Barcelona, Spain. 13. Department of Biomedical Data Science. 14. Division of Clinical Epidemiology and Aging Research. 15. Department of Epidemiology, Geisel School of Medicine, Dartmouth College, Hanover, NH. 16. Centre Hospitalier Universitaire Hotel-Dieu, Nantes, France. 17. Huntsman Cancer Institute and Department of Population Health Sciences, University of Utah, Salt Lake City, UT. 18. CESP (U1018 INSERM), Facultés de Médecine Université Paris-Sud, UVSQ, Université Paris-Saclay, Villejuif, France. 19. Gustave Roussy, Villejuif, France. 20. German Cancer Consortium. 21. National Center for Tumor Diseases (NCT), Heidelberg, Germany. 22. Service de Génétique Médicale, Centre Hospitalier Universitaire (CHU), Nantes, France. 23. Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Parkville, Victoria, Australia. 24. Colorectal Oncogenomics Group, Department of Pathology (DDB) and Genetic Epidemiology Laboratory, Department of Pathology, University of Melbourne, Melbourne, Victoria, Australia. 25. Genetic Medicine and Familial Cancer Centre, The Royal Melbourne Hospital, Parkville, Victoria, Australia. 26. Division of Research, Kaiser Permanente Medical Care Program of Northern California, Oakland, CA. 27. Epidemiology Research Program, American Cancer Society, Atlanta, GA. 28. Genetic Oncology Unit, Instituto de Investigación Sanitaria Galicia Sur (IISGS), Complejo Hospitalario Universitario de Vigo (CHUVI), SERGAS, Vigo (Pontevedra) Spain. 29. Division of Gastroenterology. 30. Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, Boston, MA. 31. Unit of Genetic Epidemiology, Division of Cancer Epidemiology. 32. Harvard Medical School, Boston, MA. 33. University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany. 34. Cancer Prevention Institute of California, Fremont, CA. 35. Ph.D. Program of Cancer Research and Drug Discovery. 36. Cancer Science Institute of Singapore, National University of Singapore, Singapore. 37. Department of Colorectal Surgery, Cleveland Clinic, Cleveland, OH. 38. Division of Environmental Health Sciences, University of Minnesota, Minneapolis, MN. 39. Van Andel Research Institute, Grand Rapids, MI. 40. Prevention and Cancer Control, Cancer Care Ontario, Toronto, ON, Canada. 41. Puerto Rico Cancer Center. 42. Genetic Basis of Human Disease Division, Translational Genomics Research Institute, Phoenix, AZ. 43. Centre for Cancer Genetic Epidemiology. 44. Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia. 45. Division of Human Nutrition, Wageningen University and Research, Wageningen, the Netherlands. 46. University of Michigan Comprehensive Cancer Center, Ann Arbor, MI. 47. Menzies Institute for Medical Research, University of Tasmania, Hobart, Tasmania, Australia. 48. W.M. Keck Science Department, Claremont Colleges, Claremont, CA. 49. Department of Biostatistics and Center for Statistical Genetics, University of Michigan School of Public Health, Ann Arbor, MI. 50. K.G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Norwegian University of Science and Technology, Trondheim, Sør-Trøndelag, Norway. 51. Department of Medical Oncology, Dana-Farber Cancer Institute, Brookline, MA. 52. Department of Medicine, Brigham and Women's Institute, Brookline, MA. 53. Genomic Medicine Group, Galician Foundation of Genomic Medicine, Complejo Hospitalario Universitario de Santiago, Servicio Galego de Saude (SERGAS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago De Compostela, Spain. 54. Moores Cancer Center, University of California San Diego, La Jolla, CA. 55. Zane Cohen Centre for Digestive Diseases, Mount Sinai Hospital, Toronto, Ontario, Canada. 56. Channing Division of Network Medicine, Brigham and Women's Institute, Brookline, MA. 57. Department of Biostatistics. 58. Unidad de Investigacion en Diabetes y Riesgo Cardiovascular, Centro de Investigacion en Salud Poblacional, Instituto Nacional de Salud Publica, Cuernavaca, Morelos, Mexico. 59. Centro de Estudios en Diabetes AC, Mexico City, Mexico. 60. Department of Medicine, Division of Gastroenterology, School of Medicine. 61. Department of Pathology, University of Michigan, Ann Arbor, MI. 62. Medical University of Vienna, Department of Medicine I, Institute of Cancer Research, Vienna, Austria. 63. Medical Department 1, University Hospital Dresden, TU Dresden, Dresden, Germany. 64. Department of Radiation Sciences, Oncology, Umea University, Umea, Sweden. 65. Division of Epidemiology, Department of Population Health, New York University School of Medicine, New York, NY. 66. Centre for MEGA Epidemiology, The University of Melbourne, Carlton, Victoria, Australia. 67. Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain. 68. AbbVie, Redwood City, CA. 69. Ontario Institute for Cancer Research, Toronto, Ontario, Canada. 70. Program in Genetic Epidemiology and Statistical Genetics, Department of Epidemiology, Harvard School of Public Health, Boston, MA. 71. Division of Epidemiology, Center for Public Health Sciences. 72. Department of Medicine, Ohio State University, Columbus, OH. 73. Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, South Korea. 74. State Key Laboratory of Oncology in South China, Cancer Center, Sun Yatsen University, Guangzhou, China. 75. Office of Public Health Studies, University of Hawaii Manoa, Honolulu, HI. 76. Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy. 77. Division of Cancer Epidemiology. 78. Department of Preventive Medicine, Kyushu University, Fukuoka, Japan. 79. Department of Medicine, University of Southern California, Los Angeles, CA. 80. Translational Research Program, Fred Hutchinson Cancer Research Center, Seattle, WA. 81. Department of Family Medicine and Community Health, Mary Ann Swetland Center for Environmental Health, Case Comprehensive Cancer Center, Case Western Reserve University, Cleveland, OH. 82. Institute of Epidemiology, PopGen Biobank, Christian-Albrechts-University Kiel, Kiel, Germany. 83. Department of Health Science Research, Mayo Clinic, Scottsdale, AZ. 84. Joint Biobank, Office of Human Research. 85. Division of Epidemiology, Vanderbilt Epidemiology Center, Vanderbilt University School of Medicine, Nashville, TN. 86. Clalit Health Services National Israeli Cancer Control Center, Haifa, Israel. 87. Harvard School of Public Health, Boston, MA. 88. Genentech, Inc., Basel, Switzerland. 89. Departments of Medicine and Genetics, Case Comprehensive Cancer Center, Case Western Reserve University, and University Hospitals of Cleveland, Cleveland, OH. 90. Biomedicine Institute (IBIOMED), University of León, León, Spain. 91. Vanderbilt-Ingram Cancer Center, Vanderbilt University, Nashville, TN. 92. Department of Epidemiology, Nagoya University Graduate School of Medicine, Showa-ku, Nagoya, Japan. 93. Division of Molecular and Clinical Epidemiology, Aichi Cancer Center Research Institute, Chikusa-Ku Nagoya, Japan. 94. Research Group on Gene-Environment Interactions and Health, University of León, León, Spain. 95. Nutrition and Metabolism Section, IARC, Lyon, CEDEX 08, France. 96. Clinical Genetics Service (KO), Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY. 97. Cancer Risk Factors and Life-Style Epidemiology Unit, Cancer Research and Prevention Institute-ISPO, Florence, Italy. 98. Department of Surgery, Complejo Hospitalario Universitario de Santiago (CHUS), Servicio Galego de Saúde (SERGAS), Santiago De Compostela, Spain. 99. Division of Cancer Biology, University of Puerto Rico, San Juan, Puerto Rico. 100. Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK. 101. Department of Community Medicine and Epidemiology, Carmel Medical Center, Haifa, Israel. 102. Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel. 103. Department of Visceral and Thoracic Surgery, University Hospital Schleswig-Holstein, Kiel Campus, Kiel, Germany. 104. Department of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, PA. 105. Epidemiology and Genomics Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, National Institutes of Health, Bethesda, MD. 106. Human Genetics Foundation (HuGeF), Torino, Italy. 107. Department of Surgery, Children's Hospital Los Angeles, Los Angeles, CA. 108. Department of Surgery, University of Tennessee Health Science Center, Memphis, TN. 109. Department of Internal Medicine, University of Utah Health Sciences Center, Salt Lake City, UT. 110. Department of Medicine, Weill Cornell Medical Center, New York, NY. 111. Department of Hematology and Oncology University of Munich (LMU), Munich, Germany. 112. Phoenix College, Phoenix, AZ. 113. Mayo Clinic, Rochester, MN. 114. Hellenic Health Foundation, Athens, Greece. 115. Department of Chronic Disease Prevention, National Institute for Health and Welfare, Helsinki, Finland. 116. Institute of Environmental Medicine. 117. Discipline of Genetics, Faculty of Medicine, Memorial University of Newfoundland, St. John's, Newfoundland, Canada. 118. Department of Nutrition, Harvard School of Public Health, Boston, MA. 119. State Key Laboratory of Oncogene and Related Genes and Department of Epidemiology, Shanghai Cancer Institute, Shanghai, China. 120. Department of Medical Oncology and Therapeutic Research, City of Hope National Medical Center, Duarte, CA. 121. Clinical Epidemiology Program, Ottawa Hospital Research Institute, Ottawa, Ontario, Canada. 122. The University of Ottawa, Ottawa, Ontario, Canada. 123. Division of Noncommunicable Disease Epidemiology and Southwest Hospital Clinical Research Center, Third Military Medical University, Chongqing, China. 124. Department of Preventive Medicine, Chonnam National University Medical School, Gwangju, South Korea. 125. South Korea Jeonnam Regional Cancer Center, Chonnam National University Hwasun Hospital, Hwasun, South Korea. 126. Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA. 127. Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA. 128. Department of Molecular Medicine and Surgery, Karolinska Institutet Solna, Stockholm, Sweden. 129. Department of Epidemiology, School of Public Health, University of Washington, Seattle, WA.
Abstract
BACKGROUND: Previous genome-wide association studies (GWAS) have identified 42 loci (P < 5 × 10-8) associated with risk of colorectal cancer (CRC). Expanded consortium efforts facilitating the discovery of additional susceptibility loci may capture unexplained familial risk. METHODS: We conducted a GWAS in European descent CRC cases and control subjects using a discovery-replication design, followed by examination of novel findings in a multiethnic sample (cumulative n = 163 315). In the discovery stage (36 948 case subjects/30 864 control subjects), we identified genetic variants with a minor allele frequency of 1% or greater associated with risk of CRC using logistic regression followed by a fixed-effects inverse variance weighted meta-analysis. All novel independent variants reaching genome-wide statistical significance (two-sided P < 5 × 10-8) were tested for replication in separate European ancestry samples (12 952 case subjects/48 383 control subjects). Next, we examined the generalizability of discovered variants in East Asians, African Americans, and Hispanics (12 085 case subjects/22 083 control subjects). Finally, we examined the contributions of novel risk variants to familial relative risk and examined the prediction capabilities of a polygenic risk score. All statistical tests were two-sided. RESULTS: The discovery GWAS identified 11 variants associated with CRC at P < 5 × 10-8, of which nine (at 4q22.2/5p15.33/5p13.1/6p21.31/6p12.1/10q11.23/12q24.21/16q24.1/20q13.13) independently replicated at a P value of less than .05. Multiethnic follow-up supported the generalizability of discovery findings. These results demonstrated a 14.7% increase in familial relative risk explained by common risk alleles from 10.3% (95% confidence interval [CI] = 7.9% to 13.7%; known variants) to 11.9% (95% CI = 9.2% to 15.5%; known and novel variants). A polygenic risk score identified 4.3% of the population at an odds ratio for developing CRC of at least 2.0. CONCLUSIONS: This study provides insight into the architecture of common genetic variation contributing to CRC etiology and improves risk prediction for individualized screening.
BACKGROUND: Previous genome-wide association studies (GWAS) have identified 42 loci (P < 5 × 10-8) associated with risk of colorectal cancer (CRC). Expanded consortium efforts facilitating the discovery of additional susceptibility loci may capture unexplained familial risk. METHODS: We conducted a GWAS in European descent CRC cases and control subjects using a discovery-replication design, followed by examination of novel findings in a multiethnic sample (cumulative n = 163 315). In the discovery stage (36 948 case subjects/30 864 control subjects), we identified genetic variants with a minor allele frequency of 1% or greater associated with risk of CRC using logistic regression followed by a fixed-effects inverse variance weighted meta-analysis. All novel independent variants reaching genome-wide statistical significance (two-sided P < 5 × 10-8) were tested for replication in separate European ancestry samples (12 952 case subjects/48 383 control subjects). Next, we examined the generalizability of discovered variants in East Asians, African Americans, and Hispanics (12 085 case subjects/22 083 control subjects). Finally, we examined the contributions of novel risk variants to familial relative risk and examined the prediction capabilities of a polygenic risk score. All statistical tests were two-sided. RESULTS: The discovery GWAS identified 11 variants associated with CRC at P < 5 × 10-8, of which nine (at 4q22.2/5p15.33/5p13.1/6p21.31/6p12.1/10q11.23/12q24.21/16q24.1/20q13.13) independently replicated at a P value of less than .05. Multiethnic follow-up supported the generalizability of discovery findings. These results demonstrated a 14.7% increase in familial relative risk explained by common risk alleles from 10.3% (95% confidence interval [CI] = 7.9% to 13.7%; known variants) to 11.9% (95% CI = 9.2% to 15.5%; known and novel variants). A polygenic risk score identified 4.3% of the population at an odds ratio for developing CRC of at least 2.0. CONCLUSIONS: This study provides insight into the architecture of common genetic variation contributing to CRC etiology and improves risk prediction for individualized screening.
Authors: Peter Broderick; Luis Carvajal-Carmona; Alan M Pittman; Emily Webb; Kimberley Howarth; Andrew Rowan; Steven Lubbe; Sarah Spain; Kate Sullivan; Sarah Fielding; Emma Jaeger; Jayaram Vijayakrishnan; Zoe Kemp; Maggie Gorman; Ian Chandler; Elli Papaemmanuil; Steven Penegar; Wendy Wood; Gabrielle Sellick; Mobshra Qureshi; Ana Teixeira; Enric Domingo; Ella Barclay; Lynn Martin; Oliver Sieber; David Kerr; Richard Gray; Julian Peto; Jean-Baptiste Cazier; Ian Tomlinson; Richard S Houlston Journal: Nat Genet Date: 2007-10-14 Impact factor: 38.330
Authors: Stephen B Gruber; Victor Moreno; Laura S Rozek; Hedy S Rennerts; Flavio Lejbkowicz; Joseph D Bonner; Joel K Greenson; Thomas J Giordano; Eric R Fearson; Gad Rennert Journal: Cancer Biol Ther Date: 2007-07 Impact factor: 4.742
Authors: Meredith Yeager; Nick Orr; Richard B Hayes; Kevin B Jacobs; Peter Kraft; Sholom Wacholder; Mark J Minichiello; Paul Fearnhead; Kai Yu; Nilanjan Chatterjee; Zhaoming Wang; Robert Welch; Brian J Staats; Eugenia E Calle; Heather Spencer Feigelson; Michael J Thun; Carmen Rodriguez; Demetrius Albanes; Jarmo Virtamo; Stephanie Weinstein; Fredrick R Schumacher; Edward Giovannucci; Walter C Willett; Geraldine Cancel-Tassin; Olivier Cussenot; Antoine Valeri; Gerald L Andriole; Edward P Gelmann; Margaret Tucker; Daniela S Gerhard; Joseph F Fraumeni; Robert Hoover; David J Hunter; Stephen J Chanock; Gilles Thomas Journal: Nat Genet Date: 2007-04-01 Impact factor: 38.330
Authors: P Lichtenstein; N V Holm; P K Verkasalo; A Iliadou; J Kaprio; M Koskenvuo; E Pukkala; A Skytthe; K Hemminki Journal: N Engl J Med Date: 2000-07-13 Impact factor: 91.245
Authors: Maria Teresa Landi; Nilanjan Chatterjee; Kai Yu; Lynn R Goldin; Alisa M Goldstein; Melissa Rotunno; Lisa Mirabello; Kevin Jacobs; William Wheeler; Meredith Yeager; Andrew W Bergen; Qizhai Li; Dario Consonni; Angela C Pesatori; Sholom Wacholder; Michael Thun; Ryan Diver; Martin Oken; Jarmo Virtamo; Demetrius Albanes; Zhaoming Wang; Laurie Burdette; Kimberly F Doheny; Elizabeth W Pugh; Cathy Laurie; Paul Brennan; Rayjean Hung; Valerie Gaborieau; James D McKay; Mark Lathrop; John McLaughlin; Ying Wang; Ming-Sound Tsao; Margaret R Spitz; Yufei Wang; Hans Krokan; Lars Vatten; Frank Skorpen; Egil Arnesen; Simone Benhamou; Christine Bouchard; Andres Metspalu; Andres Metsapalu; Tonu Vooder; Mari Nelis; Kristian Välk; John K Field; Chu Chen; Gary Goodman; Patrick Sulem; Gudmar Thorleifsson; Thorunn Rafnar; Timothy Eisen; Wiebke Sauter; Albert Rosenberger; Heike Bickeböller; Angela Risch; Jenny Chang-Claude; H Erich Wichmann; Kari Stefansson; Richard Houlston; Christopher I Amos; Joseph F Fraumeni; Sharon A Savage; Pier Alberto Bertazzi; Margaret A Tucker; Stephen Chanock; Neil E Caporaso Journal: Am J Hum Genet Date: 2009-10-15 Impact factor: 11.025
Authors: Laufey Amundadottir; Peter Kraft; Rachael Z Stolzenberg-Solomon; Charles S Fuchs; Gloria M Petersen; Alan A Arslan; H Bas Bueno-de-Mesquita; Myron Gross; Kathy Helzlsouer; Eric J Jacobs; Andrea LaCroix; Wei Zheng; Demetrius Albanes; William Bamlet; Christine D Berg; Franco Berrino; Sheila Bingham; Julie E Buring; Paige M Bracci; Federico Canzian; Françoise Clavel-Chapelon; Sandra Clipp; Michelle Cotterchio; Mariza de Andrade; Eric J Duell; John W Fox; Steven Gallinger; J Michael Gaziano; Edward L Giovannucci; Michael Goggins; Carlos A González; Göran Hallmans; Susan E Hankinson; Manal Hassan; Elizabeth A Holly; David J Hunter; Amy Hutchinson; Rebecca Jackson; Kevin B Jacobs; Mazda Jenab; Rudolf Kaaks; Alison P Klein; Charles Kooperberg; Robert C Kurtz; Donghui Li; Shannon M Lynch; Margaret Mandelson; Robert R McWilliams; Julie B Mendelsohn; Dominique S Michaud; Sara H Olson; Kim Overvad; Alpa V Patel; Petra H M Peeters; Aleksandar Rajkovic; Elio Riboli; Harvey A Risch; Xiao-Ou Shu; Gilles Thomas; Geoffrey S Tobias; Dimitrios Trichopoulos; Stephen K Van Den Eeden; Jarmo Virtamo; Jean Wactawski-Wende; Brian M Wolpin; Herbert Yu; Kai Yu; Anne Zeleniuch-Jacquotte; Stephen J Chanock; Patricia Hartge; Robert N Hoover Journal: Nat Genet Date: 2009-08-02 Impact factor: 38.330
Authors: Richard S Houlston; Emily Webb; Peter Broderick; Alan M Pittman; Maria Chiara Di Bernardo; Steven Lubbe; Ian Chandler; Jayaram Vijayakrishnan; Kate Sullivan; Steven Penegar; Luis Carvajal-Carmona; Kimberley Howarth; Emma Jaeger; Sarah L Spain; Axel Walther; Ella Barclay; Lynn Martin; Maggie Gorman; Enric Domingo; Ana S Teixeira; David Kerr; Jean-Baptiste Cazier; Iina Niittymäki; Sari Tuupanen; Auli Karhu; Lauri A Aaltonen; Ian P M Tomlinson; Susan M Farrington; Albert Tenesa; James G D Prendergast; Rebecca A Barnetson; Roseanne Cetnarskyj; Mary E Porteous; Paul D P Pharoah; Thibaud Koessler; Jochen Hampe; Stephan Buch; Clemens Schafmayer; Jurgen Tepel; Stefan Schreiber; Henry Völzke; Jenny Chang-Claude; Michael Hoffmeister; Hermann Brenner; Brent W Zanke; Alexandre Montpetit; Thomas J Hudson; Steven Gallinger; Harry Campbell; Malcolm G Dunlop Journal: Nat Genet Date: 2008-11-16 Impact factor: 38.330
Authors: Gloria M Petersen; Laufey Amundadottir; Charles S Fuchs; Peter Kraft; Rachael Z Stolzenberg-Solomon; Kevin B Jacobs; Alan A Arslan; H Bas Bueno-de-Mesquita; Steven Gallinger; Myron Gross; Kathy Helzlsouer; Elizabeth A Holly; Eric J Jacobs; Alison P Klein; Andrea LaCroix; Donghui Li; Margaret T Mandelson; Sara H Olson; Harvey A Risch; Wei Zheng; Demetrius Albanes; William R Bamlet; Christine D Berg; Marie-Christine Boutron-Ruault; Julie E Buring; Paige M Bracci; Federico Canzian; Sandra Clipp; Michelle Cotterchio; Mariza de Andrade; Eric J Duell; J Michael Gaziano; Edward L Giovannucci; Michael Goggins; Göran Hallmans; Susan E Hankinson; Manal Hassan; Barbara Howard; David J Hunter; Amy Hutchinson; Mazda Jenab; Rudolf Kaaks; Charles Kooperberg; Vittorio Krogh; Robert C Kurtz; Shannon M Lynch; Robert R McWilliams; Julie B Mendelsohn; Dominique S Michaud; Hemang Parikh; Alpa V Patel; Petra H M Peeters; Aleksandar Rajkovic; Elio Riboli; Laudina Rodriguez; Daniela Seminara; Xiao-Ou Shu; Gilles Thomas; Anne Tjønneland; Geoffrey S Tobias; Dimitrios Trichopoulos; Stephen K Van Den Eeden; Jarmo Virtamo; Jean Wactawski-Wende; Zhaoming Wang; Brian M Wolpin; Herbert Yu; Kai Yu; Anne Zeleniuch-Jacquotte; Joseph F Fraumeni; Robert N Hoover; Patricia Hartge; Stephen J Chanock Journal: Nat Genet Date: 2010-01-24 Impact factor: 38.330
Authors: Sonja Neumeyer; Katja Butterbach; Barbara L Banbury; Sonja I Berndt; Peter T Campbell; Rowan T Chlebowski; Andrew T Chan; Edward L Giovannucci; Amit D Joshi; Shuji Ogino; Mingyang Song; Marjorie L McCullough; Haifa Maalmi; JoAnn E Manson; Lori C Sakoda; Robert E Schoen; Martha L Slattery; Emily White; Aung K Win; Jane C Figueiredo; John L Hopper; Finlay A Macrae; Ulrike Peters; Hermann Brenner; Michael Hoffmeister; Polly A Newcomb; Jenny Chang-Claude Journal: Cancer Epidemiol Biomarkers Prev Date: 2020-03-18 Impact factor: 4.254
Authors: Jun Wang; Isaac Asante; John A Baron; Jane C Figueiredo; Robert Haile; A Joan Levine; Polly A Newcomb; Allyson S Templeton; Fredrick R Schumacher; Stan G Louie; Graham Casey; David V Conti Journal: Genet Epidemiol Date: 2019-09-10 Impact factor: 2.135
Authors: Kathryn L Penney; Barbara L Banbury; Stephanie Bien; Tabitha A Harrison; Xinwei Hua; Amanda I Phipps; Wei Sun; Mingyang Song; Amit D Joshi; Steven R Alberts; Carmen J Allegra; James Atkins; Linda H Colangelo; Thomas J George; Richard M Goldberg; Peter C Lucas; Suresh G Nair; Qian Shi; Frank A Sinicrope; Norman Wolmark; Greg Yothers; Ulrike Peters; Polly A Newcomb; Andrew T Chan Journal: Clin Gastroenterol Hepatol Date: 2019-12-04 Impact factor: 11.382
Authors: Peter T Campbell; Yi Lin; Stephanie A Bien; Jane C Figueiredo; Tabitha A Harrison; Mark A Guinter; Sonja I Berndt; Hermann Brenner; Andrew T Chan; Jenny Chang-Claude; Steven J Gallinger; Susan M Gapstur; Graham G Giles; Edward Giovannucci; Stephen B Gruber; Marc Gunter; Michael Hoffmeister; Eric J Jacobs; Mark A Jenkins; Loic Le Marchand; Li Li; John R McLaughlin; Neil Murphy; Roger L Milne; Polly A Newcomb; Christina Newton; Shuji Ogino; John D Potter; Gad Rennert; Hedy S Rennert; Jennifer Robinson; Lori C Sakoda; Martha L Slattery; Yiqing Song; Emily White; Michael O Woods; Graham Casey; Li Hsu; Ulrike Peters Journal: J Natl Cancer Inst Date: 2021-01-04 Impact factor: 13.506