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Soy Food Intake and Pancreatic Cancer Risk: the Japan Public Health Center-Based

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Soy Food Intake and Pancreatic Cancer Risk: the Japan Public Health Center-Based Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 1 Title: Soy food intake and pancreatic cancer risk: The Japan Public Health Center-based Prospective Study Authors: Yoko Yamagiwa1, Norie Sawada1, Taichi Shimazu1, Taiki Yamaji1, Atsushi Goto1, Ribeka Takachi2, Junko Ishihara3, Motoki Iwasaki1, Manami Inoue1, and Shoichiro Tsugane1; for the JPHC Study Group. 1 Epidemiology and Prevention Group, Center for Public Health Science, National Cancer Center, Tokyo, Japan 2 Department of Food Science and Nutrition, Faculty of Human Life and Environment, Nara Women’s University, Nara, Japan 3 Department of Food and Life Science, School of Life and Environmental Science, Azabu University, Kanagawa, Japan Running title: Soy food intake and pancreatic cancer risk Keywords: dietary factor; fermentation; Japan Public Health Center-based Prospective Study; pancreatic cancer; soy. Additional information: Grant support: National Cancer Center Research and Development Fund (since 2011), a Grant-in-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 2 Japan (from 1989 to 2010), and Ministry of Agriculture, Fishery and Forestry, Japan (MAFFCPS-2016-1-1). Corresponding author: Norie Sawada, MD, PhD Epidemiology and Prevention Group, Center for Public Health Science, National Cancer Center Mailing address: 5-1-1 Tsukiji, Chuo-ku, Tokyo, 104-0045 Japan Tel: +81-3-3547-5201 Fax: +81-3-3547-8578 E-mail: [email protected] Conflicts of interest: The authors declare no potential conflicts of interest Word count: 2808 Total number of figures and tables: One figure and four tables Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 3 Abstract Background: Although the poor prognosis and increasing incidence of pancreatic cancer highlight the need for prevention strategies, few lifestyle risk factors for pancreatic cancer have yet been identified. Soybeans contain various bioactive compounds. However, the association between soy food intake and pancreatic cancer risk remains unknown. Methods: The Japan Public Health Center-based Prospective Study (JPHC Study) is a cohort study conducted in a general Japanese population. To determine the association of soy food intake and pancreatic cancer incidence, we analyzed 90,185 participants who responded to a questionnaire on medical history and lifestyle factors, including dietary factors based on a food-frequency questionnaire in 1995–1998, using Cox proportional hazards models. Results: During a median follow-up of 16.9 years, 577 cases of pancreatic cancer were identified. In the multivariate-adjusted model, total soy food intake was statistically significantly associated with an increased risk of pancreatic cancer (hazard ratio [HR] for the highest versus lowest intake quartile: 1.48; 95% confidence interval [CI]: 1.15– 1.92; P-trend = 0.007). Among soy foods, non-fermented soy food intake showed a statistically significant positive association with pancreatic cancer (HR: 1.41; 95% CI: Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 4 1.09–1.81; P-trend = 0.008), whereas fermented soy food intake showed no association (HR: 0.96; 95% CI: 0.73–1.26; P-trend = 0.982). Conclusions: Higher intake of soy foods, particularly non-fermented soy foods, might increase pancreatic cancer risk. Impact: This study is the first to report an association between the intake of various soy foods and pancreatic cancer risk. Further studies are required to confirm our findings. Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 5 Introduction Outcomes in pancreatic cancer are hampered by a lack of reliable tests for early diagnosis and effective treatments, and the prognosis of this condition remains poor. In Japan, the 5-year survival rate was only 7.7% in 2010 (1), and mortality has now increased, ranking it as the 4th leading cause of cancer death (2). While previous epidemiological studies have identified some risk factors, including obesity, smoking, history of diabetes, history of chronic pancreatitis, and family history of pancreatic cancer (3,4), no clear prevention strategies for pancreatic cancer have yet been established. Soybeans contain various bioactive compounds, including isoflavones, polypeptides, lectins, saponins, and enzyme inhibitors. These can have both beneficial and harmful effects on human health (5,6). Soy food intake has been associated with reduced risk of chronic diseases, including cardiovascular diseases; associated risk factors, such as hyperlipidemia and hypertension (7,8); and prostate and breast cancer (8-10). In contrast, animal experiments have shown that consumption of raw soy flour causes hypertrophy, hyperplasia, and neoplasm of the pancreas in some animals (11). To our knowledge, however, only one epidemiological study has demonstrated a positive association Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 6 between intake of a soy food – miso soup – and pancreatic cancer (12). Here, we aimed to identify the association between soy food intake and pancreatic cancer risk in a large-scale, population-based prospective study in Japan. Methods Study population The Japan Public Health Center-based Prospective Study (JPHC Study) is a nationwide, population-based longitudinal study that aims to assess the risk of cancer and cardiovascular disease in the Japanese population. Details of the JPHC Study have been described elsewhere (13,14). Briefly, Cohort I in 1990–1994 and Cohort II in 1993– 1995 enrolled 140,420 baseline participants aged 40–69 years in 11 prefectural public health center (PHC) areas (Fig. 1). The starting point for this study was defined as the 5-year follow-up survey in 1995–1998 due to its more detailed estimation of dietary intake. According to the eligibility criteria, we excluded participants shown in Fig.1. Consequently, data from 90,185 participants (41,899 men and 48,286 women) were analyzed in this study. During the study period, 5,725 participants (6.3%) emigrated out of their PHC area and 104 (0.1%) were lost to follow-up. This study conformed to the Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 7 ethical guidelines of the Declaration of Helsinki. The study protocol was approved by the Institutional Review Board of the National Cancer Center, Japan (Approval number: 2001-021). Dietary assessment Dietary factors were estimated based on the average intake frequency and amount consumed relative to a standard portion size during the previous year for 138 food items using the food-frequency questionnaire (FFQ), a validated, self-administered questionnaire, as previously reported (14,15). Of these, we classified soy-based foods into the following groups: total soy foods (eight soy food items), fermented soy foods (two items: fermented soybeans [natto] and fermented soybean paste [miso]), non-fermented soy foods (six items: tofu [soy curd] in miso soup, boiled or cold tofu [yudofu, hiyayakko], pre-drained tofu [yushidofu], freeze-dried tofu [koyadofu], deep fried tofu [aburaage], and soy milk), and tofu (three items: tofu in miso soup, boiled or cold tofu, and pre-drained tofu; grouped according to similarities in the manufacturing process). Intake of genistein, an isoflavone in soy foods, was calculated based on the FFQ and the Standard Tables of Food Composition in Japan (7th revised version, 2015) (16). Intake of soy foods and genistein was adjusted for total energy intake using the Downloaded from cebp.aacrjournals.org on September 26, 2021. © 2020 American Association for Cancer Research. Author Manuscript Published OnlineFirst on March 13, 2020; DOI: 10.1158/1055-9965.EPI-19-1254 Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. 8 residual method (17), and participants were divided into quartiles of intake for each food group for analysis. Spearman’s rank correlation coefficient for total soy food intake was 0.45 for men and 0.44 for women in Cohort I (18), and 0.52 for men and 0.54 for women in Cohort II (19) in assessment of the validity of the FFQ using 28-day dietary records. Identification of pancreatic cancer Pancreatic cancer incidence was determined from medical records and population-based cancer registries in the PHC areas as previously reported (14). In accordance with the International Classification of Diseases for Oncology (Third Edition) (20), pancreatic cancer cases were determined by codes C25.0–C25.3 and C25.5–C25.9, but excluded endocrine tumor (C25.4) was excluded due to the difference in etiology.
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