Heterogeneity of Colorectal Cancer Risk Factors by Anatomical Subsite in 10 European Countries: A Multinational Cohort Study

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  • Neil Murphy, Section of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France. Electronic address: murphyn@iarc.fr., France
  • Heather A Ward, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, U.K., United Kingdom
  • Mazda Jenab, Section of Nutrition and Metabolism, International Agency for Research on Cancer (IARC), Lyon, France., France
  • Joseph A Rothwell, Section of Nutrition and Metabolism, International Agency for Research on Cancer (IARC), Lyon, France., France
  • Marie-Christine Boutron-Ruault, CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris-Saclay, 94805, Villejuif, France; Gustave Roussy, F-94805, Villejuif, France., France
  • Franck Carbonnel, CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris-Saclay, 94805, Villejuif, France; Gustave Roussy, F-94805, Villejuif, France; Department of Gastroenterology, Bicêtre University Hospital, Assistance Publique des Hôpitaux de Paris, Le Kremlin Bicêtre, France., France
  • Marina Kvaskoff, CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris-Saclay, 94805, Villejuif, France; Gustave Roussy, F-94805, Villejuif, France., France
  • Rudolf Kaaks, Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany., Germany
  • Tilman Kühn, Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany., Germany
  • Heiner Boeing, Department of Epidemiology, German Institute for Human Nutrition Potsdam-Rehbrücke, Nuthetal, Germany., Germany
  • Krasimira Aleksandrova, Nutrition, Immunity and Metabolism Start-up Lab, Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbrücke, Nuthetal, Germany., Germany
  • Elisabete Weiderpass, Department of Community Medicine, Faculty of Health Sciences, University of Tromsø, The Arctic University of Norway, Tromsø, Norway; Department of Research, Cancer Registry of Norway, Institute of Population-Based Cancer Research, Oslo, Norway; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden; Genetic Epidemiology Group, Folkhälsan Research Center, Helsinki, Finland., Norway
  • Guri Skeie, Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway., Norway
  • Kristin Benjaminsen Borch, Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway., Norway
  • Anne Tjønneland, Danish Cancer Society, Denmark
  • Cecilie Kyrø, Danish Cancer Society, Denmark
  • Kim Overvad
  • Christina C Dahm
  • Paula Jakszyn, Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology, L´Hospitallet de Llobregat, Barcelona, Spain; Facultat de Ciències de la Salut Blanquerna, Universitat Ramon Llull, Barcelona, Spain., Spain
  • Maria-Jose Sánchez, Escuela Andaluza de Salud Pública. Instituto de Investigación Biosanitaria ibs.GRANADA. Hospitales Universitarios de Granada/Universidad de Granada, Granada, Spain; CIBER de Epidemiología y Salud Pública (CIBERESP), Spain., Spain
  • Leire Gil, Public Helath Division of Gipuzkoa, Basque Health Department, BioDonostia Research Institute, San Sebastián, Spain., Spain
  • José M Huerta, Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain; CIBER de Epidemiología y Salud Pública (CIBERESP), Spain., Spain
  • Aurelio Barricarte, Navarra Public Health Institute, Pamplona, Spain; Navarra Institute for Health Research (IdiSNA) Pamplona, Spain; CIBER de Epidemiología y Salud Pública (CIBERESP), Spain., Spain
  • J Ramón Quirós, Public Health Directorate, Asturias, Spain., Spain
  • Kay-Tee Khaw, Clinical Gerontology Unit, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, Cambridge CB2 0SP, UK., United Kingdom
  • Nick Wareham, Medical Research Council Epidemiology Unit, School of Clinical Medicine, University of Cambridge, Cambridge, UK., United Kingdom
  • Kathryn E Bradbury, Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK., United Kingdom
  • Antonia Trichopoulou, Hellenic Health Foundation, Athens, Greece; WHO Collaborating Center for Nutrition and Health, Unit of Nutritional Epidemiology and Nutrition in Public Health, Department of Hygiene, Epidemiology and Medical Statistics, School of Medicine, National and Kapodistrian University of Athens, Greece., Greece
  • Carlo La Vecchia, Hellenic Health Foundation, Athens, Greece; Department of Clinical Sciences and Community Health Università degli Studi di Milano, Italy., Italy
  • Anna Karakatsani, Hellenic Health Foundation, Athens, Greece; Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, "ATTIKON" University Hospital, Haidari, Greece., Greece
  • Domenico Palli, Cancer Risk Factors and Life-Style Epidemiology Unit, Cancer Research and Prevention Institute-ISPO, 50139 Florence, Italy., Italy
  • Sara Grioni, 12 Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy., Italy
  • Rosario Tumino, Civic-M.P. Arezzo Hospital, Italy
  • Francesca Fasanelli, Unit of Cancer Epidemiology, Department of Medical Sciences, University of Turin, Turin, Italy., Italy
  • Salvatore Panico, Dipartimento di Medicina Clinica e Sperimentale, Federico II University, Naples, Italy., Italy
  • Bas Bueno-de-Mesquita, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK; Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), PO Box 1, 3720 BA Bilthoven, The Netherlands; Department of Gastroenterology and Hepatology, University Medical Centre, Utrecht, The Netherlands; Department of Social & Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia., United Kingdom
  • Petra H Peeters, Department of Epidemiology, Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, 3584 Utrecht, The Netherlands., Netherlands
  • Björn Gylling, Department of Medical Biosciences, Pathology Umeå University, 90185 Umeå, Sweden., Sweden
  • Robin Myte, Public Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden., Sweden
  • Karin Jirström, Department of Clinical Sciences Lund, Division of Oncology and Pathology, Lund University, Lund, Sweden., Sweden
  • Jonna Berntsson, Department of Clinical Sciences Lund, Division of Oncology and Pathology, Lund University, Lund, Sweden., Sweden
  • Xiaonan Xue, Albert Einstein College of Medicine, Bronx, New York, NY, U.S., United States
  • Elio Riboli, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, U.K., United Kingdom
  • Amanda J Cross, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, U.K., United Kingdom
  • Marc J Gunter, Section of Nutrition and Metabolism, International Agency for Research on Cancer (IARC), Lyon, France., France

BACKGROUND AND AIMS: Colorectal cancer located at different anatomical subsites may have distinct etiologies and risk factors. Previous studies that have examined this hypothesis have yielded inconsistent results, possibly because most have been of insufficient size to identify heterogeneous associations with precision.

METHODS: In the European Prospective Investigation into Cancer and Nutrition study, we used multivariable joint Cox proportional hazards models, which accounted for tumors at different anatomical sites (proximal colon, distal colon, and rectum) as competing risks, to examine the relationships between 14 established/suspected lifestyle, anthropometric, and reproductive/menstrual risk factors with colorectal cancer risk. Heterogeneity across sites was tested using Wald tests.

RESULTS: After 14.9 years (median) follow-up of 521,330 men and women, 6,291 colorectal cancer cases occurred. Physical activity was inversely related to proximal colon and distal colon cancer, but not to rectal cancer (P-heterogeneity=0.03). Height was positively associated with proximal and distal colon cancer only, but not rectal cancer (P-heterogeneity=0.0001). For men, but not women, heterogeneous relationships were observed for body mass index (P-heterogeneity=0.008) and waist circumference (P-heterogeneity=0.03), with weaker positive associations found for rectal cancer, compared to proximal and distal colon cancer. Current smoking was associated with a greater risk of rectal and proximal colon cancer, but not distal colon cancer (P-heterogeneity=0.05). No heterogeneity by anatomical site was found for alcohol consumption, diabetes, nonsteroidal anti-inflammatory drug use, and reproductive/menstrual factors.

CONCLUSIONS: The physical activity, anthropometry, and smoking relationships with colorectal cancer risk differed by subsite, supporting the hypothesis that tumors in different anatomical regions may have distinct etiologies.

Original languageEnglish
JournalClinical Gastroenterology and Hepatology
Volume17
Issue7
Pages (from-to)1323-1331.e6
Number of pages15
ISSN1542-3565
DOIs
Publication statusPublished - Jun 2019

    Research areas

  • colorectal cancer, anatomical subsite, distal colon, heterogeneity, proximal colon, rectum, risk factors

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