Abstract
The role of chronic inflammation on breast cancer (BC) risk remains unclear beyond as an underlying mechanism of obesity and physical activity. We aimed to evaluate the association between the inflammatory potential of the diet and risk of BC overall, according to menopausal status and tumour subtypes. Within the European Prospective Investigation into Cancer and Nutrition cohort, 318,686 women were followed for 14 years, among whom 13,246 incident BC cases were identified. The inflammatory potential of the diet was characterized by an inflammatory score of the diet (ISD). Multivariable Cox regression models were used to assess the potential effect of the ISD on BC risk by means of hazard ratios (HR) and 95% confidence intervals (CI). ISD was positively associated with BC risk. Each increase of one standard deviation (1-Sd) of the score increased by 4% the risk of BC (HR = 1.04; 95% CI 1.01–1.07). Women in the highest quintile of the ISD (indicating a most pro-inflammatory diet) had a 12% increase in risk compared with those in the lowest quintile (HR = 1.12; 95% CI 1.04–1.21) with a significant trend. The association was strongest among premenopausal women, with an 8% increased risk for 1-Sd increase in the score (HR = 1.08; 95% CI 1.01–1.14). The pattern of the association was quite homogeneous by BC subtypes based on hormone receptor status. There were no significant interactions between ISD and body mass index, physical activity, or alcohol consumption. Women consuming more pro-inflammatory diets as measured by ISD are at increased risk for BC, especially premenopausal women.
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Abbreviations
- BC:
-
Breast cancer
- BMI:
-
Body mass index
- CI:
-
Confidence interval
- DII:
-
Dietary inflammatory index
- EPIC:
-
European prospective investigation into cancer and nutrition
- ER:
-
Estrogen receptor
- HER2:
-
Human epidermal growth factor receptor 2
- HR:
-
Hazard ratio
- IARC:
-
International agency for research on cancer
- ICD-O:
-
International classification of diseases for oncology
- ISD:
-
Inflammatory score of the diet
- LR:
-
Likelihood ratio
- PR:
-
Progesterone receptor
- SD/Sd:
-
Standard deviation
References
Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.
Lim B, Woodward WA, Wang X, Reuben JM, Ueno NT. Inflammatory breast cancer biology: the tumour microenvironment is key. Nat Rev Cancer. 2018;18:485–99.
Kerr J, Anderson C, Lippman SM. Physical activity, sedentary behaviour, diet, and cancer: an update and emerging new evidence. Lancet Oncol. 2017;18:e457–71.
World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Report: Diet, Nutrition, Physical Activity and Breast Cancer; 2017. Available at wcrf.org/breast-cancer-2017. Accessed 23 July 2020.
Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, et al. Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr. 2015;114:999–1012.
Jayedi A, Emadi A, Shab-Bidar S. Dietary inflammatory index and site-specific cancer risk: a systematic review and dose-response meta-analysis. Adv Nutr. 2018;9:388–403.
Zahedi H, Djalalinia S, Sadeghi O, Asayesh H, Noroozi M, Gorabi AM, et al. Dietary inflammatory potential score and risk of breast cancer: systematic review and meta-analysis. Clin Breast Cancer. 2018;18:e561–70.
Liu ZY, Gao XP, Zhu S, Liu YH, Wang LJ, Jing CX, et al. Dietary inflammatory index and risk of gynecological cancers: a systematic review and meta-analysis of observational studies. J Gynecol Oncol. 2019;30:e23.
Shivappa N, Sandin S, Löf M, Hébert JR, Adami H-O, Weiderpass E. Prospective study of dietary inflammatory index and risk of breast cancer in Swedish women. Br J Cancer. 2015;113:1099–103.
Tabung FK, Steck SE, Liese AD, Zhang J, Ma Y, Caan B, et al. Association between dietary inflammatory potential and breast cancer incidence and death: results from the Women’s Health Initiative. Br J Cancer. 2016;114:1277–85.
Tabung FK, Steck SE, Liese AD, Zhang J, Ma Y, Johnson KC, et al. Patterns of change over time and history of the inflammatory potential of diet and risk of breast cancer among postmenopausal women. Breast Cancer Res Treat. 2016;159:139–49.
Graffouillère L, Deschasaux M, Mariotti F, Neufcourt L, Shivappa N, Hébert JR, et al. The Dietary Inflammatory Index is associated with prostate cancer risk in French middle-aged adults in a prospective study. J Nutr. 2016;146:785–91.
Shivappa N, Blair CK, Prizment AE, Jacobs DR, Hébert JR. Prospective study of the dietary inflammatory index and risk of breast cancer in postmenopausal women. Mol Nutr Food Res. 2017;61(5):1600592.
Gardeazabal I, Ruiz-Canela M, Sánchez-Bayona R, Romanos-Nanclares A, Aramendía-Beitia JM, Shivappa N, et al. Dietary inflammatory index and incidence of breast cancer in the SUN project. Clin Nutr Edinb Scotl. 2019;38:2259–68.
Park YM, Shivappa N, Petimar J, Hodgson ME, Nichols HB, Steck SE, et al. Dietary inflammatory potential, oxidative balance score, and risk of breast cancer: findings from the Sister Study. Int J Cancer. 2021. https://doi.org/10.1002/ijc.33581.
Riboli E, Hunt K, Slimani N, Ferrari P, Norat T, Fahey M, et al. European prospective investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5:1113–24.
Slimani N, Deharveng G, Unwin I, Southgate DAT, Vignat J, Skeie G, et al. The EPIC nutrient database project (ENDB): a first attempt to standardize nutrient databases across the 10 European countries participating in the EPIC study. Eur J Clin Nutr. 2007;61:1037–56.
Slimani N, Kaaks R, Ferrari P, Casagrande C, Clavel-Chapelon F, Lotze G. European Prospective Investigation into Cancer and Nutrition (EPIC) calibration study: rationale, design and population characteristics. Public Health Nutr. 2002;5:1125–45.
Agudo A, Cayssials V, Bonet C, Tjønneland A, Overvad K, Boutron-Ruault MC, et al. Inflammatory potential of the diet and risk of gastric cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Am J Clin Nutr. 2018;107:607–16.
Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17:1689–96.
Dossus L, Boutron-Ruault MC, Kaaks R, Gram IT, Vilier A, Fervers B. Active and passive cigarette smoking and breast cancer risk: results from the EPIC cohort. Int J Cancer. 2014;134:1871–88.
Hakinson SE, Polyak K, Garber JE. Breast cancer. Multiple, often complex, risk factors. In: Wild CP, Weiderpass E, Stewart BW, editors. World Cancer Report: Cancer Research for Cancer Prevention. Lyon: International Agency for Research on Cancer; 2020. p. 383–93.
Steck SE, Murphy EA. Dietary patterns and cancer risk. Nat Rev Cancer. 2020;20:125–38.
Sierksma A, van der Gaag MS, Kluft C, Hendriks HFJ. Moderate alcohol consumption reduces plasma C-reactive protein and fibrinogen levels; a randomized, diet-controlled intervention study. Eur J Clin Nutr. 2002;56:1130–6.
Imhof A, Woodward M, Doering A, Helbecque N, Loewel H, Amouyel P, et al. Overall alcohol intake, beer, wine, and systemic markers of inflammation in western Europe: results from three MONICA samples (Augsburg, Glasgow, Lille). Eur Heart J. 2004;25:2092–100.
Buckland G, Travier N, Cottet V, González CA, Luján-Barroso L, Agudo A, et al. Adherence to the mediterranean diet and risk of breast cancer in the European prospective investigation into cancer and nutrition cohort study. Int J Cancer. 2013;132:2918–27.
Renehan AG, Zwahlen M, Egger M. Adiposity and cancer risk: new mechanistic insights from epidemiology. Nat Rev Cancer. 2015;15:484–98.
McTiernan A. Mechanisms linking physical activity with cancer. Nat Rev Cancer. 2008;8:205–11.
Nadler DL, Zurbenko IG. Estimating cancer latency times using a Weibull model. Adv Epidemiol. 2014. https://doi.org/10.1155/2014/746769.
Colditz GA, Rosner BA, Chen WY, Holmes MD, Hankinson SE. Risk factors for breast cancer according to estrogen and progesterone receptor status. J Natl Cancer Inst. 2004;96:218–28.
Acknowledgements
We thank CERCA Programme/Generalitat de Catalunya for institutional support. We also thank the National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands, for their contribution and ongoing support to the EPIC Study.
Funding
This work was funded by Instituto de Salud Carlos III through the project PI15/00639 (Co-funded by European Regional Development Fund [ERDF], a way to build Europe). C. Castro-Espin was funded by Instituto de Salud Carlos III through the Grant FI19/00197 (Co-funded by European Social Fund. ESF investing in your future). The coordination of EPIC is financially supported by International Agency for Research on Cancer (IARC) and also by the Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London which has additional infrastructure support provided by the NIHR Imperial Biomedical Research Centre (BRC). 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), German Institute of Human Nutrition Potsdam-Rehbruecke (DIfE), Federal Ministry of Education and Research (BMBF) (Germany); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy, Compagnia di SanPaolo 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), Statistics Netherlands (The Netherlands); Health Research Fund (FIS)—Instituto de Salud Carlos III (ISCIII), Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, and the Catalan Institute of Oncology—ICO (Spain); Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to EPIC-Norfolk; C8221/A29017 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk; MR/M012190/1 to EPIC-Oxford) (United Kingdom). The funders of this study had no role in the decisions about the analysis or interpretation of the data; or preparation, review or approval of the manuscript.
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Castro-Espin, C., Agudo, A., Bonet, C. et al. Inflammatory potential of the diet and risk of breast cancer in the European Investigation into Cancer and Nutrition (EPIC) study. Eur J Epidemiol 36, 953–964 (2021). https://doi.org/10.1007/s10654-021-00772-2
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DOI: https://doi.org/10.1007/s10654-021-00772-2