Evidence map›Paper›PMID 30056182›Full record

ArticleClinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association2019

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

Neil Murphy, Heather A Ward, Mazda Jenab, Joseph A Rothwell, Marie-Christine Boutron-Ruault, Franck Carbonnel, Marina Kvaskoff, Rudolf Kaaks, Tilman Kühn, Heiner Boeing and 35 more

Open access · hybridAbstract readMulticenter Study
In one paragraph

Article in Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 87 papers, 8 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
87citing papers in PubMed, 8 pooled it
7.2field-weighted citation impact, top 2% 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

87 citing papers in PubMed, 8 syntheses or guidelines pooled it, 166 citations in OpenAlex.

  1. 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
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  14. Accounting for Endoscopic Screening in Colorectal Cancer Risk Models.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2025
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  17. Black-White disparities across the colorectal cancer care continuum in the USA.Nature reviews. Gastroenterology & hepatology · 2025
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27 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

45 authors at 20 institutions in 13 countries.

Neil MurphySection of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France. Electronic address: murphyn@iarc.fr.
Heather A WardDepartment of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
Mazda JenabSection of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France.
Joseph A RothwellSection of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France.
Marie-Christine Boutron-RuaultLe Centre de recherche en Epidémiologie et Santé des Populations, Faculte de Médecine, University Paris-Sud, Faculte de Médecine, Université de Versailles Saint-Quentin-en-Yvelines, INSERM, Université Paris-Saclay, Villejuif, France; Gustave Roussy, Villejuif, France.
Franck CarbonnelLe Centre de recherche en Epidémiologie et Santé des Populations, Faculte de Médecine, University Paris-Sud, Faculte de Médecine, Université de Versailles Saint-Quentin-en-Yvelines, INSERM, Université Paris-Saclay, Villejuif, France; Gustave Roussy, Villejuif, France; Department of Gastroenterology, Bicêtre University Hospital, Assistance Publique des Hôpitaux de Paris, Le Kremlin Bicêtre, France.
Marina KvaskoffLe Centre de recherche en Epidémiologie et Santé des Populations, Faculte de Médecine, University Paris-Sud, Faculte de Médecine, Université de Versailles Saint-Quentin-en-Yvelines, INSERM, Université Paris-Saclay, Villejuif, France; Gustave Roussy, Villejuif, France.
Rudolf KaaksDivision of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.
Tilman KühnDivision of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.
Heiner BoeingDepartment of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbrücke, Germany.
Krasimira AleksandrovaDepartment of Epidemiology, Nutrition, Immunity and Metabolism Start-up Laboratory, Potsdam-Rehbrücke, Germany.
Elisabete WeiderpassDepartment 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 and Faculty of Medicine, University of Helsinki, Helsinki, Finland; Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.
Guri SkeieDepartment of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.
Kristin Benjaminsen BorchDepartment of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.
Anne TjønnelandDanish Cancer Society Research Center, Copenhagen, Denmark.
Cecilie KyrøDanish Cancer Society Research Center, Copenhagen, Denmark.
Kim OvervadDepartment of Public Health, Aarhus University, Aarhus, Denmark.
Christina C DahmDepartment of Public Health, Aarhus University, Aarhus, Denmark.
Paula JakszynUnit 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.
Maria-Jose SánchezEscuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria, Hospitales Universitarios de Granada/Universidad de Granada, Granada, Spain; Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública, Madrid, Spain.
Leire GilPublic Health Division of Gipuzkoa, Research Institute of BioDonostia, San Sebastian, Spain.
José M HuertaCentro de Investigación Biomédica en Red de Epidemiología y Salud Pública, Madrid, Spain; Department of Epidemiology, Murcia Regional Health Council, Biomedical Research Institute of Murcia-Arrixaca, Murcia, Spain.
Aurelio BarricarteCentro de Investigación Biomédica en Red de Epidemiología y Salud Pública, Madrid, Spain; Navarra Public Health Institute, Pamplona, Spain; Navarra Institute for Health Research, Pamplona, Spain.
J Ramón QuirósPublic Health Directorate, Asturias, Spain.
Kay-Tee KhawUniversity of Cambridge School of Clinical Medicine, Clinical Gerontology Unit, Addenbrooke's Hospital, Cambridge, United Kingdom.
Nick WarehamMedical Research Council Epidemiology Unit, University of Cambridge School of Clinical Medicine, Cambridge, United Kingdom.
Kathryn E BradburyCancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom.
Antonia TrichopoulouHellenic Health Foundation, Athens, Greece; World Health Organization 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, Athens, Greece.
Carlo La VecchiaHellenic Health Foundation, Athens, Greece; Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milan, Italy.
Anna KarakatsaniHellenic Health Foundation, Athens, Greece; Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, Attikon University Hospital, Haidari, Greece.
Domenico PalliCancer Risk Factors and Life-Style Epidemiology Unit, Cancer Research and Prevention Institute, Cancer Research and Prevention Institute, Florence, Italy.
Sara GrioniEpidemiology and Prevention Unit, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Istituto Nazionale dei Tumori, Milan, Italy.
Rosario TuminoCancer Registry and Histopathology Department, Civic-M.P. Arezzo Hospital, Azienda Sanitaria Provinciale Ragusa, Italy.
Francesca FasanelliUnit of Cancer Epidemiology, Department of Medical Sciences, University of Turin, Turin, Italy.
Salvatore PanicoDipartimento di Medicina Clinica e Sperimentale, Federico II University, Naples, Italy.
Bas Bueno-de-MesquitaDepartment of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom; Department for Determinants of Chronic Diseases, National Institute for Public Health and the Environment (Netherlands National Institute for Public Health and the Environment), Bilthoven, The Netherlands; Department of Gastroenterology and Hepatology, University Medical Centre, Utrecht, The Netherlands; Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia.
Petra H PeetersDepartment of Epidemiology, Julius Center for Health Sciences and Primary Care, University Medical Centre, Utrecht, The Netherlands.
Björn GyllingDepartment of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden.
Robin MyteDepartment of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
Karin JirströmDivision of Oncology and Pathology, Department of Clinical Sciences, Lund University, Lund, Sweden.
Jonna BerntssonDivision of Oncology and Pathology, Department of Clinical Sciences, Lund University, Lund, Sweden.
Xiaonan XueAlbert Einstein College of Medicine, Bronx, New York, New York.
Elio RiboliDepartment of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
Amanda J CrossDepartment of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
Marc J GunterSection of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France.
Centre international de recherche sur le cancer · FRImperial College London · GBInserm · FRAarhus University · DKDanish Cancer Society · DKGerman Cancer Research Center · DEGerman Institute of Human Nutrition · DELund University · SENational and Kapodistrian University of Athens · GRUiT The Arctic University of Norway · NOUmeå University · SEUniversity Medical Center Utrecht · NLUniversity of Cambridge · GBAlbert Einstein College of Medicine · USBiogipuzkoa Health Research Institute · ESFondazione IRCCS Istituto Nazionale dei Tumori · ITGobierno del Principado de Asturias · ESInstitut Català d'Oncologia · ESInstituto de Salud Pública de Navarra · ESInstituto Murciano de Investigación Biosanitaria · ES

Funding

Cancer Research UK 14136Cancer Research UK 25004Cancer Research UK A16491Cancer Research UK C8221/A19170Medical Research Council G0401527Medical Research Council G1000143Medical Research Council MC_UU_12015/1Medical Research Council MR/M012190/1Medical Research Council MR/N003284/1World Health Organization 001
6 · The paper itself

Abstract

BACKGROUND &

aimsColorectal 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 studies have been of insufficient size to identify heterogeneous associations with precision.

methodsIn 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.

resultsAfter a median of 14.9 years of follow-up of 521,330 men and women, 6291 colorectal cancer cases occurred. Physical activity was related inversely to proximal colon and distal colon cancer, but not to rectal cancer (P heterogeneity = .03). Height was associated positively with proximal and distal colon cancer only, but not rectal cancer (P heterogeneity = .0001). For men, but not women, heterogeneous relationships were observed for body mass index (P heterogeneity = .008) and waist circumference (P heterogeneity = .03), with weaker positive associations found for rectal cancer, compared with 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 = .05). No heterogeneity by anatomical site was found for alcohol consumption, diabetes, nonsteroidal anti-inflammatory drug use, and reproductive/menstrual factors.

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

Indexed as

ExerciseLife StyleAdultAlcohol DrinkingColonColonoscopyColorectal NeoplasmsEuropeFemaleFollow-Up StudiesHumansIncidenceMaleMiddle AgedProspective StudiesRectumAnatomic SubsiteColorectal CancerDistal ColonHeterogeneityProximal ColonRectumRisk Factors

Identifiers

PMID30056182
PMCPMC6542674
OpenAlexW2883015258

What OpenQuestion holds

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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.