Abstract
Purpose
To evaluate the role of a diabetes risk reduction diet (DRRD) on pancreatic cancer risk.
Methods
We used data from a hospital-based case–control study conducted in Italy between 1991 and 2008; the study included 326 incident pancreatic cancer cases and 652 controls matched by age, gender and study center. Subjects’ usual diet was collected through a valid and reproducible food frequency questionnaire. A DRRD score was derived from 8 dietary components: cereal fiber, total fruit, coffee, polyunsaturated to saturated fats ratio and nuts (higher score for higher intake), and dietary glycemic index, red/processed meat and sugar-sweetened beverages/fruit juices (higher score for lower intake). The score ranged 8–37, with higher values indicating greater DRRD adherence. Odds ratios (ORs) of pancreatic cancer according to the DRRD score were estimated using multiple conditional logistic regression models.
Results
After allowance for confounding factors, the DRRD score was inversely related to pancreatic cancer risk, with ORs of 0.55 (95% confidence interval, CI 0.38–0.80) for the highest versus the lowest score tertile (p for trend across tertiles = 0.002) and 0.84 (95% CI 0.75–0.95) for a 3-point score increment. The exclusion of diabetic subjects and additional adjustment for vegetable intake did not change the results. Inverse associations were observed in subgroups defined by age, gender, education, body mass index, smoking and total energy intake.
Conclusion
Study findings suggest a protective role of high adherence to a DRRD on pancreatic cancer risk.
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Availability of data and material
The dataset used and analyzed during the current study is available from the corresponding author on reasonable request.
Code availability
SAS code is available from the corresponding author on reasonable request.
References
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492
Lucas AL, Malvezzi M, Carioli G, Negri E, La Vecchia C, Boffetta P, Bosetti C (2016) Global trends in pancreatic cancer mortality from 1980 through 2013 and predictions for 2017. Clin Gastroenterol Hepatol 14:1452-1462 e1454. https://doi.org/10.1016/j.cgh.2016.05.034
Huang J, Lok V, Ngai CH, Zhang L, Yuan J, Lao XQ, Ng K, Chong C, Zheng ZJ, Wong MCS (2020) Worldwide burden of, risk factors for, and trends in pancreatic cancer. Gastroenterology. https://doi.org/10.1053/j.gastro.2020.10.007
Ferlay J, Partensky C, Bray F (2016) More deaths from pancreatic cancer than breast cancer in the EU by 2017. Acta Oncol 55:1158–1160. https://doi.org/10.1080/0284186X.2016.1197419
Bosetti C, Lucenteforte E, Silverman DT, Petersen G, Bracci PM, Ji BT, Negri E, Li D, Risch HA, Olson SH, Gallinger S, Miller AB, Bueno-de-Mesquita HB, Talamini R, Polesel J, Ghadirian P, Baghurst PA, Zatonski W, Fontham E, Bamlet WR, Holly EA, Bertuccio P, Gao YT, Hassan M, Yu H, Kurtz RC, Cotterchio M, Su J, Maisonneuve P, Duell EJ, Boffetta P, La Vecchia C (2012) Cigarette smoking and pancreatic cancer: an analysis from the International Pancreatic Cancer Case-Control Consortium (Panc4). Ann Oncol 23:1880–1888. https://doi.org/10.1093/annonc/mdr541
Midha S, Chawla S, Garg PK (2016) Modifiable and non-modifiable risk factors for pancreatic cancer: a review. Cancer Lett 381:269–277. https://doi.org/10.1016/j.canlet.2016.07.022
Bosetti C, Rosato V, Li D, Silverman D, Petersen GM, Bracci PM, Neale RE, Muscat J, Anderson K, Gallinger S, Olson SH, Miller AB, Bas Bueno-de-Mesquita H, Scelo G, Janout V, Holcatova I, Lagiou P, Serraino D, Lucenteforte E, Fabianova E, Baghurst PA, Zatonski W, Foretova L, Fontham E, Bamlet WR, Holly EA, Negri E, Hassan M, Prizment A, Cotterchio M, Cleary S, Kurtz RC, Maisonneuve P, Trichopoulos D, Polesel J, Duell EJ, Boffetta P, La Vecchia C, Ghadirian P (2014) Diabetes, antidiabetic medications, and pancreatic cancer risk: an analysis from the international pancreatic cancer case–control consortium. Ann Oncol 25:2065–2072. https://doi.org/10.1093/annonc/mdu276
Pannala R, Basu A, Petersen GM, Chari ST (2009) New-onset diabetes: a potential clue to the early diagnosis of pancreatic cancer. Lancet Oncol 10:88–95. https://doi.org/10.1016/S1470-2045(08)70337-1
Pizzato M, Turati F, Rosato V, La Vecchia C (2019) Exploring the link between diabetes and pancreatic cancer. Expert Rev Anticancer Ther 19:681–687. https://doi.org/10.1080/14737140.2019.1642109
Andersen DK, Korc M, Petersen GM, Eibl G, Li D, Rickels MR, Chari ST, Abbruzzese JL (2017) Diabetes, pancreatogenic diabetes, and pancreatic cancer. Diabetes 66:1103–1110. https://doi.org/10.2337/db16-1477
World Cancer Research Fund/American Institute for Cancer Research. Continuous update project expert report 2018. Diet, nutrition, physical activity and pancreatic cancer. https://www.wcrf.org/diet-and-cancer/
Wu QJ, Wu L, Zheng LQ, Xu X, Ji C, Gong TT (2016) Consumption of fruit and vegetables reduces risk of pancreatic cancer: evidence from epidemiological studies. Eur J Cancer Prev 25:196–205. https://doi.org/10.1097/CEJ.0000000000000171
Rossi M, Lugo A, Lagiou P, Zucchetto A, Polesel J, Serraino D, Negri E, Trichopoulos D, La Vecchia C (2012) Proanthocyanidins and other flavonoids in relation to pancreatic cancer: a case–control study in Italy. Ann Oncol 23:1488–1493. https://doi.org/10.1093/annonc/mdr475
Zheng J, Guinter MA, Merchant AT, Wirth MD, Zhang J, Stolzenberg-Solomon RZ, Steck SE (2017) Dietary patterns and risk of pancreatic cancer: a systematic review. Nutr Rev 75:883–908. https://doi.org/10.1093/nutrit/nux038
Bosetti C, Turati F, Dal Pont A, Ferraroni M, Polesel J, Negri E, Serraino D, Talamini R, La Vecchia C, Zeegers MP (2013) The role of Mediterranean diet on the risk of pancreatic cancer. Br J Cancer 109:1360–1366. https://doi.org/10.1038/bjc.2013.345
Hu J, La Vecchia C, Augustin LS, Negri E, de Groh M, Morrison H, Mery L, Canadian Cancer Registries Epidemiology Research G (2013) Glycemic index, glycemic load and cancer risk. Ann Oncol 24:245–251. https://doi.org/10.1093/annonc/mds235
Rossi M, Lipworth L, Polesel J, Negri E, Bosetti C, Talamini R, McLaughlin JK, La Vecchia C (2010) Dietary glycemic index and glycemic load and risk of pancreatic cancer: a case–control study. Ann Epidemiol 20:460–465. https://doi.org/10.1016/j.annepidem.2010.03.018
Rhee JJ, Mattei J, Hughes MD, Hu FB, Willett WC (2015) Dietary diabetes risk reduction score, race and ethnicity, and risk of type 2 diabetes in women. Diabetes Care 38:596–603. https://doi.org/10.2337/dc14-1986
Kang JH, Peng C, Rhee JJ, Farvid MS, Willett WC, Hu FB, Rosner BA, Tamimi R, Eliassen AH (2020) Prospective study of a diabetes risk reduction diet and the risk of breast cancer. Am J Clin Nutr. https://doi.org/10.1093/ajcn/nqaa268
Luo X, Sui J, Yang W, Sun Q, Ma Y, Simon TG, Liang G, Meyerhardt JA, Chan AT, Giovannucci EL, Zhang X (2019) Type 2 Diabetes Prevention Diet and Hepatocellular Carcinoma Risk in US Men and Women. Am J Gastroenterol 114:1870–1877. https://doi.org/10.14309/ajg.0000000000000450
Polesel J, Talamini R, Negri E, Bosetti C, Boz G, Lucenteforte E, Franceschi S, Serraino D, La Vecchia C (2010) Dietary habits and risk of pancreatic cancer: an Italian case-control study. Cancer Causes Control 21:493–500. https://doi.org/10.1007/s10552-009-9480-2
Gnagnarella P, Parpinel M, Salvini S, Franceschi S, Palli D, Boyle P (2004) The update of the Italian food composition database. J Food Comp Analysis 17:509–522
Atkinson FS, Foster-Powell K, Brand-Miller JC (2008) International tables of glycemic index and glycemic load values: 2008. Diabetes Care 31:2281–2283. https://doi.org/10.2337/dc08-1239
Brighenti F, Casiraghi M (1992) Influenza dei processi di trasformazione sulla risposta glicemica di alimenti amidacei. G Ital Nutrizione Clin Prev 1:79–87
Decarli A, Franceschi S, Ferraroni M, Gnagnarella P, Parpinel MT, La Vecchia C, Negri E, Salvini S, Falcini F, Giacosa A (1996) Validation of a food-frequency questionnaire to assess dietary intakes in cancer studies in Italy. Results for specific nutrients. Ann Epidemiol 6:110–118. https://doi.org/10.1016/1047-2797(95)00129-8
Franceschi S, Negri E, Salvini S, Decarli A, Ferraroni M, Filiberti R, Giacosa A, Talamini R, Nanni O, Panarello G et al (1993) Reproducibility of an Italian food frequency questionnaire for cancer studies: results for specific food items. Eur J Cancer 29A:2298–2305. https://doi.org/10.1016/0959-8049(93)90225-5
Franceschi S, Barbone F, Negri E, Decarli A, Ferraroni M, Filiberti R, Giacosa A, Gnagnarella P, Nanni O, Salvini S et al (1995) Reproducibility of an Italian food frequency questionnaire for cancer studies. Results for specific nutrients. Ann Epidemiol 5:69–75. https://doi.org/10.1016/1047-2797(95)92893-d
Zhao Z, Yu P, Feng X, Yin Z, Wang S, Qiu Z, Zhao Q (2018) No associations between fruit and vegetable consumption and pancreatic cancer risk: a meta-analysis of prospective studies. Oncotarget 9:32250–32261. https://doi.org/10.18632/oncotarget.23128
Koushik A, Spiegelman D, Albanes D, Anderson KE, Bernstein L, van den Brandt PA, Bergkvist L, English DR, Freudenheim JL, Fuchs CS, Genkinger JM, Giles GG, Goldbohm RA, Horn-Ross PL, Mannisto S, McCullough ML, Millen AE, Miller AB, Robien K, Rohan TE, Schatzkin A, Shikany JM, Stolzenberg-Solomon RZ, Willett WC, Wolk A, Ziegler RG, Smith-Warner SA (2012) Intake of fruits and vegetables and risk of pancreatic cancer in a pooled analysis of 14 cohort studies. Am J Epidemiol 176:373–386. https://doi.org/10.1093/aje/kws027
Lei Q, Zheng H, Bi J, Wang X, Jiang T, Gao X, Tian F, Xu M, Wu C, Zhang L, Li N, Li J (2016) Whole grain intake reduces pancreatic cancer risk: a meta-analysis of observational studies. Med (Baltimore) 95:e2747. https://doi.org/10.1097/MD.0000000000002747
Wang CH, Qiao C, Wang RC, Zhou WP (2015) Dietary fiber intake and pancreatic cancer risk: a meta-analysis of epidemiologic studies. Sci Rep 5:10834. https://doi.org/10.1038/srep10834
Stolzenberg-Solomon RZ, Pietinen P, Taylor PR, Virtamo J, Albanes D (2002) Prospective study of diet and pancreatic cancer in male smokers. Am J Epidemiol 155:783–792. https://doi.org/10.1093/aje/155.9.783
Koulouris AI, Luben R, Banim P, Hart AR (2019) Dietary fiber and the risk of pancreatic cancer. Pancreas 48:121–125. https://doi.org/10.1097/MPA.0000000000001191
Bidoli E, Pelucchi C, Zucchetto A, Negri E, Dal Maso L, Polesel J, Boz G, Montella M, Franceschi S, Serraino D, La Vecchia C, Talamini R (2012) Fiber intake and pancreatic cancer risk: a case–control study. Ann Oncol 23:264–268. https://doi.org/10.1093/annonc/mdr060
MacMahon B, Yen S, Trichopoulos D, Warren K, Nardi G (1981) Coffee and cancer of the pancreas. N Engl J Med 304:630–633. https://doi.org/10.1056/NEJM198103123041102
Clavel F, Benhamou E, Auquier A, Tarayre M, Flamant R (1989) Coffee, alcohol, smoking and cancer of the pancreas: a case–control study. Int J Cancer 43:17–21. https://doi.org/10.1002/ijc.2910430105
Turati F, Galeone C, Edefonti V, Ferraroni M, Lagiou P, La Vecchia C, Tavani A (2012) A meta-analysis of coffee consumption and pancreatic cancer. Ann Oncol 23:311–318. https://doi.org/10.1093/annonc/mdr331
Zhou CD, Kuan AS, Reeves GK, Green J, Floud S, Beral V, Yang TO (2019) Coffee and pancreatic cancer risk among never-smokers in the UK prospective Million Women Study. Int J Cancer 145:1484–1492. https://doi.org/10.1002/ijc.31994
Obon-Santacana M, Lujan-Barroso L, Freisling H, Naudin S, Boutron-Ruault MC, Mancini FR, Rebours V, Kuhn T, Katzke V, Boeing H, Tjonneland A, Olsen A, Overvad K, Lasheras C, Rodriguez-Barranco M, Amiano P, Santiuste C, Ardanaz E, Khaw KT, Wareham NJ, Schmidt JA, Aune D, Trichopoulou A, Thriskos P, Peppa E, Masala G, Grioni S, Tumino R, Panico S, Bueno-de-Mesquita B, Sciannameo V, Vermeulen R, Sonestedt E, Sund M, Weiderpass E, Skeie G, Gonzalez CA, Riboli E, Duell EJ (2020) Consumption of nuts and seeds and pancreatic ductal adenocarcinoma risk in the European prospective investigation into cancer and nutrition. Int J Cancer 146:76–84. https://doi.org/10.1002/ijc.32415
Bao Y, Hu FB, Giovannucci EL, Wolpin BM, Stampfer MJ, Willett WC, Fuchs CS (2013) Nut consumption and risk of pancreatic cancer in women. Br J Cancer 109:2911–2916. https://doi.org/10.1038/bjc.2013.665
Nieuwenhuis L, van den Brandt PA (2018) Total nut, tree nut, peanut, and peanut butter consumption and the risk of pancreatic cancer in the netherlands cohort study. Cancer Epidemiol Biomarkers Prev 27:274–284. https://doi.org/10.1158/1055-9965.EPI-17-0448
Yao X, Tian Z (2015) Saturated, monounsaturated and polyunsaturated fatty acids intake and risk of pancreatic cancer: evidence from observational studies. PLoS ONE 10:e0130870. https://doi.org/10.1371/journal.pone.0130870
Matejcic M, Lesueur F, Biessy C, Renault AL, Mebirouk N, Yammine S, Keski-Rahkonen P, Li K, Hemon B, Weiderpass E, Rebours V, Boutron-Ruault MC, Carbonnel F, Kaaks R, Katzke V, Kuhn T, Boeing H, Trichopoulou A, Palli D, Agnoli C, Panico S, Tumino R, Sacerdote C, Quiros JR, Duell EJ, Porta M, Sanchez MJ, Chirlaque MD, Barricarte A, Amiano P, Ye W, Peeters PH, Khaw KT, Perez-Cornago A, Key TJ, Bueno-de-Mesquita HB, Riboli E, Vineis P, Romieu I, Gunter MJ, Chajes V (2018) Circulating plasma phospholipid fatty acids and risk of pancreatic cancer in a large European cohort. Int J Cancer 143:2437–2448. https://doi.org/10.1002/ijc.31797
Ghamarzad Shishavan N, Mohamadkhani A, Ghajarieh Sepanlou S, Masoudi S, Sharafkhah M, Poustchi H, Hekmatdoost A, Pourshams A (2020) Circulating plasma fatty acids and risk of pancreatic cancer: results from the Golestan Cohort Study. Clin Nutr. https://doi.org/10.1016/j.clnu.2020.09.002
Turati F, Galeone C, Augustin LSA, La Vecchia C (2019) Glycemic index, glycemic load and cancer risk: an updated meta-analysis. Nutrients. https://doi.org/10.3390/nu11102342
Milajerdi A, Larijani B, Esmaillzadeh A (2019) Sweetened beverages consumption and pancreatic cancer: a meta-analysis. Nutr Cancer 71:375–384. https://doi.org/10.1080/01635581.2019.1578390
McCullough ML, Jacobs EJ, Shah R, Campbell PT, Wang Y, Hartman TJ, Gapstur SM (2018) Meat consumption and pancreatic cancer risk among men and women in the Cancer Prevention Study-II Nutrition Cohort. Cancer Causes Control 29:125–133. https://doi.org/10.1007/s10552-017-0984-x
Zhao Z, Yin Z, Pu Z, Zhao Q (2017) Association between consumption of red and processed meat and pancreatic cancer risk: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 15:486-493 e410. https://doi.org/10.1016/j.cgh.2016.09.143
Hu FB (2002) Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol 13:3–9. https://doi.org/10.1097/00041433-200202000-00002
Michels KB, Schulze MB (2005) Can dietary patterns help us detect diet-disease associations? Nutr Res Rev 18:241–248. https://doi.org/10.1079/NRR2005107
InterAct C (2015) Dietary fibre and incidence of type 2 diabetes in eight European countries: the EPIC-InterAct Study and a meta-analysis of prospective studies. Diabetologia 58:1394–1408. https://doi.org/10.1007/s00125-015-3585-9
Hu Y, Ding M, Sampson L, Willett WC, Manson JE, Wang M, Rosner B, Hu FB, Sun Q (2020) Intake of whole grain foods and risk of type 2 diabetes: results from three prospective cohort studies. BMJ 370:m2206. https://doi.org/10.1136/bmj.m2206
Afshin A, Micha R, Khatibzadeh S, Mozaffarian D (2014) Consumption of nuts and legumes and risk of incident ischemic heart disease, stroke, and diabetes: a systematic review and meta-analysis. Am J Clin Nutr 100:278–288. https://doi.org/10.3945/ajcn.113.076901
Li S, Miao S, Huang Y, Liu Z, Tian H, Yin X, Tang W, Steffen LM, Xi B (2015) Fruit intake decreases risk of incident type 2 diabetes: an updated meta-analysis. Endocrine 48:454–460. https://doi.org/10.1007/s12020-014-0351-6
Salmeron J, Hu FB, Manson JE, Stampfer MJ, Colditz GA, Rimm EB, Willett WC (2001) Dietary fat intake and risk of type 2 diabetes in women. Am J Clin Nutr 73:1019–1026. https://doi.org/10.1093/ajcn/73.6.1019
Ding M, Bhupathiraju SN, Chen M, van Dam RM, Hu FB (2014) Caffeinated and decaffeinated coffee consumption and risk of type 2 diabetes: a systematic review and a dose-response meta-analysis. Diabetes Care 37:569–586. https://doi.org/10.2337/dc13-1203
Livesey G, Taylor R, Livesey HF, Buyken AE, Jenkins DJA, Augustin LSA, Sievenpiper JL, Barclay AW, Liu S, Wolever TMS, Willett WC, Brighenti F, Salas-Salvado J, Bjorck I, Rizkalla SW, Riccardi G, Vecchia CL, Ceriello A, Trichopoulou A, Poli A, Astrup A, Kendall CWC, Ha MA, Baer-Sinnott S, Brand-Miller JC (2019) Dietary glycemic index and load and the risk of type 2 diabetes: a systematic review and updated meta-analyses of prospective cohort studies. Nutrients. https://doi.org/10.3390/nu11061280
Imamura F, O’Connor L, Ye Z, Mursu J, Hayashino Y, Bhupathiraju SN, Forouhi NG (2015) Consumption of sugar sweetened beverages, artificially sweetened beverages, and fruit juice and incidence of type 2 diabetes: systematic review, meta-analysis, and estimation of population attributable fraction. BMJ 351:h3576. https://doi.org/10.1136/bmj.h3576
Yang X, Li Y, Wang C, Mao Z, Zhou W, Zhang L, Fan M, Cui S, Li L (2020) Meat and fish intake and type 2 diabetes: dose-response meta-analysis of prospective cohort studies. Diabetes Metab 46:345–352. https://doi.org/10.1016/j.diabet.2020.03.004
Slimani N, Deharveng G, Southgate DA, Biessy C, Chajes V, van Bakel MM, Boutron-Ruault MC, McTaggart A, Grioni S, Verkaik-Kloosterman J, Huybrechts I, Amiano P, Jenab M, Vignat J, Bouckaert K, Casagrande C, Ferrari P, Zourna P, Trichopoulou A, Wirfalt E, Johansson G, Rohrmann S, Illner AK, Barricarte A, Rodriguez L, Touvier M, Niravong M, Mulligan A, Crowe F, Ocke MC, van der Schouw YT, Bendinelli B, Lauria C, Brustad M, Hjartaker A, Tjonneland A, Jensen AM, Riboli E, Bingham S (2009) Contribution of highly industrially processed foods to the nutrient intakes and patterns of middle-aged populations in the European Prospective Investigation into Cancer and Nutrition study. Eur J Clin Nutr 63(Suppl 4):S206-225. https://doi.org/10.1038/ejcn.2009.82
Michaud DS, Giovannucci E, Willett WC, Colditz GA, Fuchs CS (2003) Dietary meat, dairy products, fat, and cholesterol and pancreatic cancer risk in a prospective study. Am J Epidemiol 157:1115–1125. https://doi.org/10.1093/aje/kwg098
Heinen MM, Verhage BA, Goldbohm RA, van den Brandt PA (2009) Meat and fat intake and pancreatic cancer risk in the Netherlands Cohort Study. Int J Cancer 125:1118–1126. https://doi.org/10.1002/ijc.24387
Hu J, La Vecchia C, de Groh M, Negri E, Morrison H, Mery L, Canadian Cancer Registries Epidemiology Research G (2011) Dietary transfatty acids and cancer risk. Eur J Cancer Prev 20:530–538. https://doi.org/10.1097/CEJ.0b013e328348fbfb
Laake I, Carlsen MH, Pedersen JI, Weiderpass E, Selmer R, Kirkhus B, Thune I, Veierod MB (2013) Intake of trans fatty acids from partially hydrogenated vegetable and fish oils and ruminant fat in relation to cancer risk. Int J Cancer 132:1389–1403. https://doi.org/10.1002/ijc.27737
Thiebaut AC, Jiao L, Silverman DT, Cross AJ, Thompson FE, Subar AF, Hollenbeck AR, Schatzkin A, Stolzenberg-Solomon RZ (2009) Dietary fatty acids and pancreatic cancer in the NIH-AARP diet and health study. J Natl Cancer Inst 101:1001–1011. https://doi.org/10.1093/jnci/djp168
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Fondazione AIRC, Associazione Italiana per la Ricerca sul cancro, Milano; FIRC, Fondazione Italiana Ricerca sul Cancro.
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FT analyzed the data and drafted the manuscript; CLV and EN conducted research; CLV, EN, MR and FB contributed substantially to the interpretation of data; all authors contributed to manuscript revision and approved the final version of the manuscript.
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Turati, F., Rossi, M., Mattioli, V. et al. Diabetes risk reduction diet and the risk of pancreatic cancer. Eur J Nutr 61, 309–316 (2022). https://doi.org/10.1007/s00394-021-02646-5
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DOI: https://doi.org/10.1007/s00394-021-02646-5