IJC International Journal of Cancer

Total, caffeinated and decaffeinated coffee and tea intake and gastric cancer risk: Results from the EPIC cohort study Harinakshi Sanikini1,2,3*, Vincent K. Dik1*, Peter D. Siersema1, Nirmala Bhoo-Pathy4,5, Cuno S.P.M. Uiterwaal6, lez7, Raul Zamora-Ros7,8, Kim Overvad9, Anne Tjïnneland10, Nina Roswall10, Petra H.M. Peeters6, Carlos A. Gonza 3,11,12 €hn13, Verena Katzke13, Marie-Christine Boutron-Ruault , Guy Fagherazzi3,11,12, Antoine Racine3,11,12, Tilman Ku 14 15,16 15,16,17 16,17,18 Heiner Boeing , Antonia Trichopoulou , Dimitrios Trichopoulos , Pagona Lagiou , Domenico Palli19, 20 21,22 23 24 25,26,27,28 Sara Grioni , Paolo Vineis , Rosario Tumino , Salvatore Panico , Elisabete Weiderpass , Guri Skeie25, 25 29,30 29,31 29,32  Marıa Huerta nchez-Cantalejo Tonje Braaten , Jose , Emilio Sa , Aurelio Barricarte , Emily Sonestedt33, 33 34 35 36 Peter Wallstrom , Lena Maria Nilsson , Ingegerd Johansson , Kathryn E Bradbury , Kay-Tee Khaw37, Nick Wareham38, Inge Huybrechts8, Heinz Freisling8, Amanda J. Cross22, Elio Riboli22 and H. B(as) Bueno-de-Mesquita1,22,39 1

Department of Gastroenterology and Hepatology, University Medical Centre Utrecht, Utrecht, The Netherlands Inserm, Centre for research in Epidemiology and Population Health (CESP), U1018, Environmental Epidemiology of Cancer Team, Villejuif, Paris, France 3 Univ Paris Sud, UMRS 1018, Villejuif, Paris, France 4 Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia 5 National Clinical Research Centre, Kuala Lumpur Hospital, Kuala Lumpur, Malaysia 6 Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht, The Netherlands 7 Unit of Nutrition, Environment and Cancer, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain 8 International Agency for Research on Cancer (IARC-WHO), Lyon, France 9 Department of Public Health, Section for Epidemiology, Aarhus University, Aarhus, Denmark 10 Danish Cancer Society Research Center, Copenhagen, Denmark 11 Inserm, Centre for Research in Epidemiology and Population Health (CESP), U1018, Nutrition, Hormones and Women’s Health team, Villejuif, Paris, France 12 IGR, Villejuif, Paris, France 13 Division of Cancer Epidemiology, German Cancer Research Centre (DKFZ), Heidelberg, Germany 14 €r Ern€ahrungsforschung, Potsdam-Rehbru €cke, Nuthetal, Germany Department of Epidemiology, Deutsches Institut fu 15 Hellenic Health Foundation, Athens, Greece 16 Bureau of Epidemiologic Research, Academy of Athens, Athens, Greece 17 Department of Epidemiology, Harvard School of Public Health, Boston, MA 18 Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Goudi, Athens, Greece 19 Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute—ISPO, Florence, Italy 20 Epidemiology and Prevention Unit, Fondazione IRCCS, Istituto Nazionale dei Tumori via Venezian 1, Milano, Italy 21 HuGeF Foundation, Torino, Italy 22 Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom 23 Cancer Registry and Histopathology Unit, Civic—M.P. Arezzo Hospital, ASP Ragusa, Italy

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Key words: coffee, caffeinated coffee, decaffeinated coffee, tea, gastric cancer, European Prospective Investigation into Cancer and Nutrition Abbreviations: EPIC: European Prospective Investigation into Cancer and Nutrition; BMI: body mass index; HR: hazard ratio; CI: confidence intervals Additional Supporting Information may be found in the online version of this article. *H.S. and V.K.D. contributed equally to this work Grant sponsors: European Commission (DG-SANCO), The International Agency for Research on Cancer, The Health Research Fund (FIS) of the Spanish Ministry of Health (Exp P10710130), La Caixa (BM 06-130), RTICC-RD06/0020/0091, RTICC-RD12/0036/0018; Regional Governments of Andalucıa, Asturias, Basque Country, Murcia (no. 6236), Navarra and the Catalan Institute of Oncology (Spain); Danish Cancer Society (Denmark); Ligue contre le Cancer, Institut Gustave Roussy, Mutuelle Generale de l’Education Nationale, Institut National de la Sante et de la Recherche Medicale (INSERM) (France), Deutsche Krebshilfe, Deutsches Krebsforschungszentrum and Federal Ministry of Education and Research (Germany); the Hellenic Health Foundation (Greece); Italian Association for Research on Cancer (AIRC) 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); Swedish Cancer Society, Swedish Scientific Council and Regional Government of Skåne and V€asterbotten (Sweden); Cancer Research UK, Medical Research Council (United Kingdom) DOI: 10.1002/ijc.29223 History: Received 17 June 2014; Accepted 15 Aug 2014; Online 18 Sep 2014 Correspondence to: H. B. Bueno-de-Mesquita, National Institute for Public Health and the Environment (RIVM), Antonie van Leeuwenhoeklaan 9, Bilthoven, P.O. Box 1, 3720 BA Bilthoven, The Netherlands, Tel.: 131-0-30-274-2019, Fax: 131-0-30-274-4466, E-mail: [email protected]

C 2014 UICC Int. J. Cancer: 136, E720–E730 (2015) V

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Dipartimento Di Medicina Clinica E Chirurgia Federico II University, Naples, Italy Department of Community Medicine, Faculty of Health Sciences, UiT The Arctic University of Norway, Tromsï, Norway 26 Department of Research, Cancer Registry of Norway, Oslo, Norway 27 Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden 28 Samfundet Folkh€alsan, Helsinki, Finland 29 blica (CIBERESP), Madrid, Spain CIBER Epidemiologıa y Salud Pu 30 Department of Epidemiology, Murcia Regional Health Council, Murcia, Spain 31 n Biosanitaria de Granada (Granada.ibs), Granada, Spain blica, Instituto de Investigacio Escuela Andaluza de Salud Pu 32 Navarre Public Health Institute, Pamplona, Spain 33 €, Sweden Nutrition Epidemiology Research Group, Department of Clinical Sciences, , Lund University, Malmo 34 Division of Nutritional Research & Arcum, Department of Public Health and Clinical Medicine, Arctic Research Centre at Umea˚ University, Umea˚, Sweden 35 Department of Odontology, Umea˚ University, Umea˚, Sweden 36 Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom 37 University of Cambridge School of Clinical Medicine, Cambridge, United Kingdom 38 University of Cambridge, MRC Epidemiology Unit, Cambridge, United Kingdom 39 National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands 25

What’s new? Can drinking coffee or tea lead to cancer? Can they protect against cancer? These popular drinks certainly contain antioxidants, but despite many investigations into the question, we still have no clear answer. A new study has plied the data from the European Prospective Investigation into Cancer and Nutrition (EPIC) in search of a link. Participants self-reported their coffee and tea consumption by questionnaire. The authors found no link between drinking tea or coffee – with or without caffeine – and overall risk of gastric cancer; they did discern a slight increase in gastric cardia cancer with consumption of caffeinated coffee.

Global incidence rates of gastric cancer have substantially declined over the past few decades. Nevertheless, gastric cancer is the fourth most common cancer and the second leading cause of cancer related death worldwide, with an estimated 990,000 gastric cancer cases and 738,000 deaths in 2008.1 More than 90% of gastric cancers are adenocarcinomas and the remaining are either lymphomas or leiomysarcomas.2 Gastric adenocarcinomas are classified by tumor site (cardia and noncardia) and histological type (diffuse and intestinal).3 The inciC 2014 UICC Int. J. Cancer: 136, E720–E730 (2015) V

dence of gastric cancer varies by geographic location, calendar time and socioeconomic status. These variations suggest that environmental exposures and lifestyle factors are major contributors to the etiology of gastric cancer.4 A comprehensive review of epidemiological evidence revealed consistent evidence for factors that contribute to an increasing risk of gastric cancer including Helicobacter Pylori infection, smoking, obesity, low consumption of fruit and vegetables and high consumption of alcohol, salted food and red and processed meat.5–17

Epidemiology

Prospective studies examining the association between coffee and tea consumption and gastric cancer risk have shown inconsistent results. We investigated the association between coffee (total, caffeinated and decaffeinated) and tea consumption and the risk of gastric cancer by anatomical site and histological type in the European Prospective Investigation into Cancer and Nutrition study. Coffee and tea consumption were assessed by dietary questionnaires at baseline. Adjusted hazard ratios (HRs) were calculated using Cox regression models. During 11.6 years of follow up, 683 gastric adenocarcinoma cases were identified among 477,312 participants. We found no significant association between overall gastric cancer risk and consumption of total coffee (HR 1.09, 95%-confidence intervals [CI]: 0.84–1.43; quartile 4 vs. non/quartile 1), caffeinated coffee (HR 1.14, 95%-CI: 0.82–1.59; quartile 4 vs. non/quartile 1), decaffeinated coffee (HR 1.07, 95%-CI: 0.75–1.53; tertile 3 vs. non/ tertile 1) and tea (HR 0.81, 95%-CI: 0.59–1.09; quartile 4 vs. non/quartile 1). When stratified by anatomical site, we observed a significant positive association between gastric cardia cancer risk and total coffee consumption per increment of 100 mL/ day (HR 1.06, 95%-CI: 1.03–1.11). Similarly, a significant positive association was observed between gastric cardia cancer risk and caffeinated coffee consumption (HR 1.98, 95%-CI: 1.16–3.36, p-trend50.06; quartile 3 vs. non/quartile 1) and per increment of 100 mL/day (HR 1.09, 95%-CI: 1.04–1.14). In conclusion, consumption of total, caffeinated and decaffeinated coffee and tea is not associated with overall gastric cancer risk. However, total and caffeinated coffee consumption may be associated with an increased risk of gastric cardia cancer. Further prospective studies are needed to rule out chance or confounding.

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Total, caffeinated and decaffeinated coffee and tea intake and gastric cancer risk

Coffee and tea are the most popular beverages consumed worldwide. In 2009, the European population consumed on average 4.68 kg per capita of coffee and 0.51 kg per capita of tea.18,19 Hence, there is a great interest in the possible role of coffee and tea on human health. Coffee and tea contain numerous substances with potentially anti-mutagenic and antioxidant activities that may play a protective role against cancer including phenolic acids and diterpenes (kahweol and cafestol) in coffee and flavonoids (flavanols and flavonols), lignans and phenolic acids in tea.20–23 Epidemiological studies that examined the association between either coffee or tea consumption and gastric cancer risk have shown inconclusive results. Although some case–control and cohort studies indicated no association between coffee consumption and risk of gastric cancer,24–26 others have shown an inverse association or a positive association.27–29 A meta-analysis (2006) of 23 studies reported no significant association between coffee consumption and gastric cancer risk.30 For black tea, two case–control studies reported an inverse association between black tea consumption and gastric cancer risk,31,32 while cohort studies revealed a positive association33,34 or no association.35,36 A recent meta-analysis by Kang et al., reported an inverse association between green tea consumption and gastric cancer risk in 11 case–control studies (RR: 0.74, 95%confidence intervals [CI]: 0.63, 0.86) and no association in seven cohort studies (RR: 1.03, 95%-CI: 0.92–1.16).37 The etiology of gastric cancers differs by tumor localization and histological type.4 However, studies examining the association between coffee and tea consumption and gastric cancer risk by tumor localization and histological type are limited.38,39 In addition, to our knowledge, no cohort studies have examined the independent associations with caffeinated and decaffeinated coffee. As coffee is a major source of caffeine and the amount of caffeine varies by processing methods, potential differences may exist between caffeinated and decaffeinated coffee in relation to gastric cancer risk. For instance, the caffeine content in decaffeinated coffee is reduced to 0.1% or less in roasted coffee beans and 0.3% or less in the instant coffee process compared to caffeinated coffee.40 Hence, we aimed to examine the association between total coffee, caffeinated coffee, decaffeinated coffee and tea consumption and the risk of gastric cancer according to anatomical site (cardia and non-cardia) and histological type (diffuse and intestinal) in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort.

Material and Methods Study population

The EPIC study is an on-going multi-center prospective cohort study aimed at investigating the association between diet, lifestyle, genetic and environmental factors and the development of cancer and other chronic diseases. The methodological details and rationale of the EPIC study have been described previously.41,42 Briefly, 521,448 participants mainly

aged 25270 years were recruited between 1992 and 2000 in 23 centers located in ten European countries including Denmark, France, Germany, Greece, Italy, Norway, Spain, Sweden, The Netherlands and United Kingdom. The participants were asked to complete questionnaires about their diet, lifestyle and medical history. All participants signed an informed consent form and the study was approved by the ethical review committees of the International Agency for Research on Cancer (IARC) and EPIC centers. For this study, we excluded 28,268 participants with prevalent cancer at recruitment or who were lost during followup and 15,868 participants for whom no dietary information was available or were in the top or bottom 1% of the ratio of energy intake to estimated energy requirement. After the exclusions, the final sample used for the analysis included 477,312 participants. Diet and lifestyle questionnaires

Usual diet was assessed at recruitment using validated country specific dietary questionnaires reflecting intake in the past 12 months. A separate questionnaire on lifestyle factors was used to collect information on smoking and alcohol consumption, education, occupation, reproductive history, family history and physical activity. Anthropometric measurements were taken at recruitment by trained health professionals in most centers, except for most of the Oxford cohort, the Norwegian cohort, and approximately two-thirds of the French cohort, in which height and weight were self-reported. More details on questionnaires can be found elsewhere.41,42 Assessment of coffee and tea intake

The consumption of coffee and tea in millilitres (mL) per day was calculated for each center separately and was based on the recorded number of cups per day, week or month depending on the exact questions per center. The structure and availability of questions differed by country and questionnaire. As a result, data on tea intake were not available for Norway. Data on both caffeinated and decaffeinated coffee were only available for France, Germany, Italy (Florence, Varese and Turin only), The Netherlands, Sweden (Malm€o only) and the United Kingdom. Cohort-wide quartiles (total coffee, caffeinated coffee and tea) or tertiles (decaffeinated coffee) for levels of consumption were computed after excluding non-consumers. Follow up and identification of cancer cases

Population-based cancer registries as well as postal follow-up questionnaires are used in most of the countries to identify incident cancer cases. In France, Germany, Greece and Naples (Italy) cancer cases are additionally identified through active follow up. Data on mortality and movement of participants are obtained through periodic linkage to regional and national mortality registries. The outcome of interest of this study was first incidence, primary gastric cancer and included cancers coded as C16 in the tenth Revision of International C 2014 UICC Int. J. Cancer: 136, E720–E730 (2015) V

Statistical Classification of Diseases, Injuries and Causes of Death (ICD). A total of 892 gastric cancer cases had been reported to IARC up to September 2010. The majority of gastric cancer cases were validated and confirmed for anatomic localization (cardia C16.0 and non-cardia C16.1–16.6) and histological type (diffuse and intestinal) by a panel of pathologists.43 Of the total gastric cancer cases, we excluded subjects with prevalent cancer at recruitment or lost to follow-up (n 5 50), no dietary information (n 5 27), gastric lymphoma (n 5 41) and other non-adenocarcinomas (n 5 91), resulting in a remaining sample of 683 gastric adenocarcinoma cases.

quartiles of total coffee, caffeinated coffee and tea consumption and tertiles of decaffeinated coffee consumption were calculated by assigning the median value to each quartile or tertile of consumption as a continuous term in the Cox regression models. To investigate possible reverse causation, sensitivity analysis was performed by excluding gastric cancer cases diagnosed in the first 2 years of follow up. The analyses were also done using country-specific cut-off points instead of cohort-wide cut-off points. All analyses were conducted by SAS 9.2 software (SAS Institute, Cary, NC) and a p-value

Total, caffeinated and decaffeinated coffee and tea intake and gastric cancer risk: results from the EPIC cohort study.

Prospective studies examining the association between coffee and tea consumption and gastric cancer risk have shown inconsistent results. We investiga...
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