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Cancer Epidemiology, Biomarkers & Prevention
Cancer Epidemiology, Biomarkers & Prevention
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Null Results in Brief

Socioeconomic Effect of Education on Pancreatic Cancer Risk in Western Europe: An Update on the EPIC Cohorts Study

Lluís Cirera, José María Huerta, María Dolores Chirlaque, Kim Overvad, Martin Lindström, Sara Regnér, Anne Tjønneland, Marie-Christine Boutron-Ruault, Vinciane Rebours, Guy Fagherazzi, Verena A. Katzke, Heiner Boeing, Eleni Peppa, Antonia Trichopoulou, Elissavet Valanou, Domenico Palli, Sara Grioni, Salvatore Panico, Rosario Tumino, Fulvio Ricceri, Carla van Gils, Roel C.H. Vermeulen, Guri Skeie, Tonje Braaten, Elisabete Weiderpass, Susana Merino, María José Sánchez, Nerea Larrañaga, Eva Ardanaz, Malin Sund, Kay-Tee Khaw, Timothy J. Key, Mazda Jenab, Sabine Naudin, Neil Murphy, Dagfinn Aune, Heather Ward, Elio Riboli, Bas Bueno-de-Mesquita, Carmen Navarro and Eric J. Duell
Lluís Cirera
1Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain.
2CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
3Department of Health and Social Sciences, University of Murcia, Murcia, Spain.
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  • For correspondence: luis.cirera@carm.es
José María Huerta
1Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain.
2CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
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María Dolores Chirlaque
1Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain.
2CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
3Department of Health and Social Sciences, University of Murcia, Murcia, Spain.
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Kim Overvad
4Department of Public Health, Aarhus University, Aarhus, Denmark.
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Martin Lindström
5Department of Clinical Sciences, Social Medicine and Health Policy, Lund University, Malmö, Sweden.
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Sara Regnér
5Department of Clinical Sciences, Social Medicine and Health Policy, Lund University, Malmö, Sweden.
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  • ORCID record for Sara Regnér
Anne Tjønneland
6Diet, Genes and Environment, Danish Cancer Society Research Center, Copenhagen, Denmark.
7Department of Public Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
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Marie-Christine Boutron-Ruault
8CESP, Faculté de Médecine - Université Paris-Sud, Faculté de Médecine - UVSQ, INSERM, Université Paris-Saclay, Villejuif, France.
9Gustave Roussy Institute, Villejuif, France.
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Vinciane Rebours
10Pancreatology Unit, Beaujon Hospital, Clichy, France.
11INSERM - UMR 1149, University Paris 7, France.
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Guy Fagherazzi
8CESP, Faculté de Médecine - Université Paris-Sud, Faculté de Médecine - UVSQ, INSERM, Université Paris-Saclay, Villejuif, France.
9Gustave Roussy Institute, Villejuif, France.
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Verena A. Katzke
12German Cancer Research Center (DKFZ), Heidelberg, Germany.
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Heiner Boeing
13Department of Epidemiology German Institute of Human Nutrition (DIfE), Potsdam-Rehbrücke, Germany.
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Eleni Peppa
14Hellenic Health Foundation, Athens, Greece.
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Antonia Trichopoulou
14Hellenic Health Foundation, Athens, Greece.
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Elissavet Valanou
14Hellenic Health Foundation, Athens, Greece.
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Domenico Palli
15Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network - ISPRO, Florence, Italy.
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Sara Grioni
16Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milano, Italy.
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Salvatore Panico
17Dipartimento di Medicina Clinica e Chirurgia, Federico ii University, Naples, Italy.
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Rosario Tumino
18Department of Cancer Registry and Histopathology, "Civic - M.P. Arezzo" Hospital, ASP Ragusa, Italy.
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Fulvio Ricceri
19Department of Clinical and Biological Sciences, University of Turin, Italy.
20Unit of Epidemiology, Regional Health Service ASL TO3, Grugliasco (TO), Italy.
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Carla van Gils
21Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands.
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Roel C.H. Vermeulen
21Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands.
22Environmental Epidemiology Division, Institute for Risk Assessment Sciences, Utrecht University, Utrecht, the Netherlands.
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Guri Skeie
23Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.
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Tonje Braaten
23Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.
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Elisabete Weiderpass
23Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.
24Department of Research, Cancer Registry of Norway, Institute of Population-Based Cancer Research, Oslo, Norway.
25Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
26Genetic Epidemiology Group, Folkhälsan Research Center, and Faculty of Medicine, Helsinki University, Helsinki, Finland.
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Susana Merino
27Public Health Directorate, Regional Government of Asturias, Oviedo, Spain.
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María José Sánchez
28Escuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria ibs.GRANADA, Hospitales Universitarios de Granada/Universidad de Granada, Granada, Spain.
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Nerea Larrañaga
2CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
29Public Health Division of Gipuzkoa, Regional Government of the Basque Country, Donostia, Spain.
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Eva Ardanaz
2CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
30Navarra Public Health Institute, Pamplona, Spain.
31IdiSNA, Navarra Institute for Health Research, Pamplona, Spain.
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Malin Sund
32Department of Public Health, Aarhus University, Aarhus, Denmark.
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Kay-Tee Khaw
33University of Cambridge, School of Clinical Medicine Addenbrooke's Hospital, Cambridge, United Kingdom.
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Timothy J. Key
34Nuffield Department of Population Health, Cancer Epidemiology Unit, University of Oxford, Oxford, United Kingdom.
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Mazda Jenab
35Section of Nutrition and Metabolism, International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Sabine Naudin
35Section of Nutrition and Metabolism, International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Neil Murphy
35Section of Nutrition and Metabolism, International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Dagfinn Aune
36Department of Epidemiology and Biostatistics, Faculty of Medicine, School of Public Health, Imperial College London, United Kingdom.
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Heather Ward
36Department of Epidemiology and Biostatistics, Faculty of Medicine, School of Public Health, Imperial College London, United Kingdom.
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Elio Riboli
36Department of Epidemiology and Biostatistics, Faculty of Medicine, School of Public Health, Imperial College London, United Kingdom.
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Bas Bueno-de-Mesquita
37Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.
38Department of Gastroenterology and Hepatology, University Medical Centre, Utrecht, the Netherlands.
39Department of Epidemiology and Biostatistics, Faculty of Medicine, School of Public Health, Imperial College London, United Kingdom.
40Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia.
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Carmen Navarro
3Department of Health and Social Sciences, University of Murcia, Murcia, Spain.
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Eric J. Duell
41Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO-IDIBELL), L’Hospitalet de Llobregat, Spain.
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DOI: 10.1158/1055-9965.EPI-18-1153 Published June 2019
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Abstract

Background: To analyze the potential effect of social inequality on pancreatic cancer risk in Western Europe, by reassessing the association within the European Prospective Investigation into Cancer and Nutrition (EPIC) Study, including a larger number of cases and an extended follow-up.

Methods: Data on highest education attained were gathered for 459,170 participants (70% women) from 10 European countries. A relative index of inequality (RII) based on adult education was calculated for comparability across countries and generations. Cox regression models were applied to estimate relative inequality in pancreatic cancer risk, stratifying by age, gender, and center, and adjusting for known pancreatic cancer risk factors.

Results: A total of 1,223 incident pancreatic cancer cases were included after a mean follow-up of 13.9 (±4.0) years. An inverse social trend was found in models adjusted for age, sex, and center for both sexes [HR of RII, 1.27; 95% confidence interval (CI), 1.02–1.59], which was also significant among women (HR, 1.42; 95% CI, 1.05–1.92). Further adjusting by smoking intensity, alcohol consumption, body mass index, prevalent diabetes, and physical activity led to an attenuation of the RII risk and loss of statistical significance.

Conclusions: The present reanalysis does not sustain the existence of an independent social inequality influence on pancreatic cancer risk in Western European women and men, using an index based on adult education, the most relevant social indicator linked to individual lifestyles, in a context of very low pancreatic cancer survival from (quasi) universal public health systems.

Impact: The results do not support an association between education and risk of pancreatic cancer.

Introduction

The incidence and mortality of pancreatic cancer have undergone a parallel rise in Europe and North America in the last decades (1). Meanwhile, pancreatic cancer 5-year survival is among the lowest of the common cancers (7%), and treatment advances have been minimal, despite the high-quality and near-universal coverage of health systems in Western Europe.

It is established that most pancreatic cancer are noninherited, although family history also conveys a higher disease risk (2). Nevertheless, little is known on the etiopathogenesis of pancreatic cancer, and effective screening tests are lacking.

Previous literature suggests a causal role for body fatness and, probably, adult height, where an evidence for alcohol, red or processed meat, and other dietary factors is limited or inconclusive (2). The established pancreatic cancer risk factors are tobacco smoking, body mass index (BMI), diabetes, and chronic pancreatitis (3).

Social determinants are linked to lifestyle cancer risk factors. However, a preceding study on the association of pancreatic cancer with socioeconomic status within the European Prospective Investigation into Cancer and Nutrition (EPIC) was inconclusive (4). This is the reason why we reanalyze this association including a larger number of cases and a longer follow-up using updated end-point data from the EPIC cohorts.

Materials and Methods

Details on study methods and sample characteristics can be found elsewhere (4, 5). EPIC recruited volunteers from 10 European countries between 1992 and 2000, who were 35 to 70 years old at baseline. A relative index of inequality (RII) was estimated on the basis of an educational ranking of individuals within each sex, age groups, and center (4). Of the 491,992 participants without prevalent cancer, those without baseline lifestyle or dietary information (n = 6,259), extreme energy reporters (n = 9,573), and individuals with missing data on education (n = 16,931, including 19 pancreatic cancer cases) were excluded. Furthermore, participants who developed a different primary cancer prior to a pancreatic and neuroendocrine cancer (n = 54) or nonmalignant tumors (n = 5) were censored at the date of the event, leaving a final sample of 457,947 noncases and 1,223 pancreatic cancer cases, with a mean follow-up of 13.9 (± 4.0) years and 6,401,413 person-years (Supplementary Table S1).

The RII was estimated through Cox regression with age as the time variable. Effect modification was evaluated by sex, age, BMI, smoking, alcohol, diabetes, and European region. Interactions were assessed using likelihood ratio tests. Sensitivity analyses were conducted to test the robustness of results against potential biases due to reverse causation or residual confounding.

Analyses were conducted using R version 3.3.2, and two-sided P values <0.05 were considered statistically significant.

Results

Table 1 shows baseline participants' characteristics by the educational ranks of RII. An inverse and statistically significant social trend was found in models adjusted for age, sex, and center for both sexes combined [HR of RII, 1.27; 95% confidence interval (CI), 1.02–1.59], which was stronger among women (HR, 1.42; 95% CI, 1.05–1.92; Table 2). Multivariate adjustment attenuated RII estimates causing the loss of statistical significance. Results were similar when considering education as the exposure.

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Table 1.

Baseline participants' characteristics in the EPIC Study by the RII

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Table 2.

Association between education and the RII with pancreatic cancer in the EPIC Cohorts Study

There was no effect modification in stratified analysis (Supplementary table S2). Sensitivity analyses adding new variables or excluding participants caused minor attenuations, which remained not significant (Supplementary table S2). Country-wise exclusion of participants resulted in a significant RII when excluding the Netherlands (RII, 1.29; 95% CI, 1.02–1.63; Supplementary table S3).

Discussion

Education is the most common individual measure of social position because it allows classifying all individuals from young adulthood. Our results do not endorse a social stratification of pancreatic cancer risk in Western Europe, after accounting for major potential confounders.

We cannot discard plausible generation effects and misclassification due to the differences across educational systems. Furthermore, the assumption that all educational categories are hierarchically ordered is not always straightforward, as for vocational and secondary education. However, the alternative use of education as the exposure and the sensitivity analyses conducted exhibited similar associations, supporting the robustness of results. Grouping secondary and vocational education did not result in higher pancreatic cancer risk (Table 2), and the comparison of extreme levels (university versus primary or lower) was not significant either.

Our results are in agreement with an earlier study evaluating the occupational status of United Kingdom's government employees, which did not obtain a significant risk of pancreatic cancer among the least affluent (6). On the contrary, a cohort study performed in Norway found higher risk of pancreatic cancer in farmers versus low occupational groups, which did not change after lifestyle adjustments (7).

Among the limitations, we had no data on developmental factors affecting linear growth (2). Nevertheless, a previous case–control study evaluating serum insulin-like growth factor I (IGF-I) and IGFBP-3 concentrations was unable to support a role for the IGF signaling axis on pancreatic cancer risk (8). Finally, we did not have information on family history (pancreatic cancer is more frequent among family members). However, it is established that over 90% of incident pancreatic cancers are sporadic (mainly attributable to genetic mutations or epigenetic dysregulation), and not inherited.

Conclusions

These results do not support an association between education and risk of pancreatic cancer.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Authors' Contributions

Conception and design: L. Cirera, J.M. Huerta, M.-D. Chirlaque, K. Overvad, A. Tjonneland, M.-C. Boutron-Ruault, H. Boeing, R. Tumino, E. Weiderpass, N. Larrañaga, K.-T. Khaw, M. Jenab, B. Bueno-de-Mesquita

Development of methodology: L. Cirera, J.M. Huerta, M.-D. Chirlaque, E. Weiderpass, N. Larrañaga, M. Jenab, B. Bueno-de-Mesquita

Acquisition of data (provided animals, acquired and managed patients, provided facilities, etc.): M.-D. Chirlaque, K. Overvad, M. Lindstrom, S. Regner, A. Tjonneland, M.-C. Boutron-Ruault, V. Rebours, G. Fagherazzi, H. Boeing, A. Trichopoulou, D. Palli, S. Panico, R. Tumino, F. Ricceri, R. Vermeulen, G. Skeie, E. Weiderpass, S. Merino, M.J. Sánchez, N. Larrañaga, M. Sund, K.-T. Khaw, T.J. Key, B. Bueno-de-Mesquita, C. Navarro

Analysis and interpretation of data (e.g., statistical analysis, biostatistics, computational analysis): L. Cirera, J.M. Huerta, M.-D. Chirlaque, E. Weiderpass, N. Larrañaga, B. Bueno-de-Mesquita

Writing, review, and/or revision of the manuscript: L. Cirera, J.M. Huerta, M.-D. Chirlaque, K. Overvad, M. Lindstrom, S. Regner, A. Tjonneland, M.-C. Boutron-Ruault, G. Fagherazzi, V.A. Katzke, H. Boeing, E. Peppa, A. Trichopoulou, D. Palli, S. Grioni, S. Panico, R. Tumino, F. Ricceri, C. van Gils, R. Vermeulen, G. Skeie, T. Braaten, E. Weiderpass, M.J. Sánchez, N. Larrañaga, M. Sund, K.-T. Khaw, T.J. Key, M. Jenab, S. Naudin, N. Murphy, D. Aune, H.A. Ward, E. Riboli, B. Bueno-de-Mesquita, C. Navarro, E.J. Duell

Administrative, technical, or material support (i.e., reporting or organizing data, constructing databases): S. Regner, H. Boeing, R. Tumino, E. Weiderpass, N. Larrañaga, K.-T. Khaw

Study supervision: L. Cirera, M.-D. Chirlaque, R. Tumino, E. Weiderpass, N. Larrañaga, B. Bueno-de-Mesquita, C. Navarro

Acknowledgments

The authors would like to thank all EPIC cohort-participants, logistic staff, and scientists for their contribution to the study. The coordination of EPIC is financially supported by the European Commission (DG-SANCO) and the International Agency for Research on Cancer (IARC). The national cohorts are supported by Danish Cancer Society (Denmark); Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l’Education Nationale, Institut National de la Santé et de la Recherche Médicale (INSERM; France); German Cancer Aid, German Cancer Research Center (DKFZ), Federal Ministry of Education and Research (BMBF), Deutsche Krebshilfe, Deutsches Krebsforschungszentrum, and Federal Ministry of Education and Research (Germany); the Hellenic Health Foundation (Greece); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy and National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports (VWS), Netherlands Cancer Registry (NKR), LK Research Funds, Dutch Prevention Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF), and Statistics Netherlands (the Netherlands); ERC-2009-AdG 232997 and Nordforsk, Nordic Centre of Excellence programme on Food, Nutrition and Health (Norway); Health Research Fund (FIS), PI13/00061 to Granada; PI13/01162 to EPIC-Murcia, Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, ISCIII RETIC (RD06/0020; Spain); Swedish Cancer Society, Swedish Research Council, and County Councils of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to EPIC-Norfolk; C570/A16491 and C8221/A19170 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk, MR/M012190/1 to EPIC-Oxford; United Kingdom).

Footnotes

  • Note: Supplementary data for this article are available at Cancer Epidemiology, Biomarkers & Prevention Online (http://cebp.aacrjournals.org/).

  • Cancer Epidemiol Biomarkers Prev 2019;28:1089–92

  • Received October 31, 2018.
  • Revision received March 5, 2019.
  • Accepted March 7, 2019.
  • Published first June 3, 2019.
  • ©2019 American Association for Cancer Research.

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Cancer Epidemiology Biomarkers & Prevention: 28 (6)
June 2019
Volume 28, Issue 6
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Socioeconomic Effect of Education on Pancreatic Cancer Risk in Western Europe: An Update on the EPIC Cohorts Study
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Socioeconomic Effect of Education on Pancreatic Cancer Risk in Western Europe: An Update on the EPIC Cohorts Study
Lluís Cirera, José María Huerta, María Dolores Chirlaque, Kim Overvad, Martin Lindström, Sara Regnér, Anne Tjønneland, Marie-Christine Boutron-Ruault, Vinciane Rebours, Guy Fagherazzi, Verena A. Katzke, Heiner Boeing, Eleni Peppa, Antonia Trichopoulou, Elissavet Valanou, Domenico Palli, Sara Grioni, Salvatore Panico, Rosario Tumino, Fulvio Ricceri, Carla van Gils, Roel C.H. Vermeulen, Guri Skeie, Tonje Braaten, Elisabete Weiderpass, Susana Merino, María José Sánchez, Nerea Larrañaga, Eva Ardanaz, Malin Sund, Kay-Tee Khaw, Timothy J. Key, Mazda Jenab, Sabine Naudin, Neil Murphy, Dagfinn Aune, Heather Ward, Elio Riboli, Bas Bueno-de-Mesquita, Carmen Navarro and Eric J. Duell
Cancer Epidemiol Biomarkers Prev June 1 2019 (28) (6) 1089-1092; DOI: 10.1158/1055-9965.EPI-18-1153

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Socioeconomic Effect of Education on Pancreatic Cancer Risk in Western Europe: An Update on the EPIC Cohorts Study
Lluís Cirera, José María Huerta, María Dolores Chirlaque, Kim Overvad, Martin Lindström, Sara Regnér, Anne Tjønneland, Marie-Christine Boutron-Ruault, Vinciane Rebours, Guy Fagherazzi, Verena A. Katzke, Heiner Boeing, Eleni Peppa, Antonia Trichopoulou, Elissavet Valanou, Domenico Palli, Sara Grioni, Salvatore Panico, Rosario Tumino, Fulvio Ricceri, Carla van Gils, Roel C.H. Vermeulen, Guri Skeie, Tonje Braaten, Elisabete Weiderpass, Susana Merino, María José Sánchez, Nerea Larrañaga, Eva Ardanaz, Malin Sund, Kay-Tee Khaw, Timothy J. Key, Mazda Jenab, Sabine Naudin, Neil Murphy, Dagfinn Aune, Heather Ward, Elio Riboli, Bas Bueno-de-Mesquita, Carmen Navarro and Eric J. Duell
Cancer Epidemiol Biomarkers Prev June 1 2019 (28) (6) 1089-1092; DOI: 10.1158/1055-9965.EPI-18-1153
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