NOTICE: We are experiencing technical issues with Academy members trying to log into the JAND site using Academy member login credentials. We are working to resolve the issue as soon as possible. Alternatively, if you are an Academy member, you can access the JAND site by registering for an Elsevier account and claiming access using the links at the top of the JAND site. Email us at [email protected] for assistance. Thanks for your patience!

Phenolic Acid Subclasses, Individual Compounds, and Breast Cancer Risk in a Mediterranean Cohort: The SUN Project

Published:January 22, 2020DOI:https://doi.org/10.1016/j.jand.2019.11.007

      Abstract

      Background

      Biological and epidemiological evidence supports an inverse association of phenolic acids with obesity-related chronic diseases. However, no previous study has prospectively evaluated the relationship between subclasses and individual compounds of phenolic acids and the risk of postmenopausal breast cancer, one of the most important and prevalent obesity-related cancer sites.

      Objective

      This study examined associations between subclasses of phenolic acids, including hydroxycinnamic and hydroxybenzoic acids intake, and risk of breast cancer.

      Design

      The Seguimiento Universidad de Navarra (SUN) Project is a dynamic, permanently open prospective cohort which started in 1999.

      Participants/setting

      Participants were 10,812 middle-aged women. All of them were university graduates.

      Main outcome measures

      Usual diet was assessed at baseline and after 10 years of follow-up with a 136-item food frequency questionnaire. Phenolic acid intake was calculated by matching food consumption with the Phenol-Explorer database on phenolic acids content of each reported food item.

      Statistical analysis performed

      Participants were classified according to tertiles of subclasses or individual compounds of phenolic acids. Cox regression models were fitted to estimate multivariable-adjusted hazard ratios and 95% CIs for breast cancer incidence.

      Results

      Over an average of 11.8 years of follow-up, 101 incident cases of breast cancer were confirmed. After multivariable adjustment, an inverse association between hydroxycinnamic acids intake and breast cancer was observed (hazard ratio third tertile vs first tertile 0.37, 95% CI 0.16 to 0.85; P for trend=0.029) among postmenopausal women. Specifically, chlorogenic acids (3-, 4-, and 5- caffeoylquinic acids) showed the strongest inverse association (hazard ratio third tertile vs first tertile 0.33, 95% CI 0.14 to 0.78; P for trend=0.012).

      Conclusions

      A higher intake of hydroxycinnamic acids, especially from chlorogenic acids—present in coffee, fruits, and vegetables—was associated with a lower incidence of breast cancer among postmenopausal women. Future observational studies are needed to corroborate these results.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Academy of Nutrition and Dietetics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bray F.
        • Ferlay J.
        • Soerjomataram I.
        • Siegel R.L.
        • Torre L.A.
        • Jemal A.
        Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA Cancer J Clin. 2018; 68: 394-424
        • Sauter E.R.
        Breast cancer prevention: Current approaches and future directions.
        Eur J Breast Health. 2018; 14: 64-71
        • World Cancer Research Fund, American Institute for Cancer Research
        Diet, nutrition, physical activity and breast cancer.
        (Accessed December 17, 2019)
        • Kang N.J.
        • Shin S.H.
        • Lee H.J.
        • Lee K.W.
        Polyphenols as small molecular inhibitors of signaling cascades in carcinogenesis.
        Pharmacol Ther. 2011; 130: 310-324
        • Del Rio D.
        • Rodriguez-Mateos A.
        • Spencer J.P.E.
        • Tognolini M.
        • Borges G.
        • Crozier A.
        Dietary (poly)phenolics in human health: Structures, bioavailability, and evidence of protective effects against chronic diseases.
        Antioxid Redox Signal. 2013; 18: 1818-1892
        • Pérez-Jiménez J.
        • Neveu V.
        • Vos F.
        • Scalbert A.
        Systematic analysis of the content of 502 polyphenols in 452 foods and beverages: An application of the phenol-explorer database.
        J Agric Food Chem. 2010; 58: 4959-4969
        • Zamora-Ros R.
        • Touillaud M.
        • Rothwell J.A.
        • Romieu I.
        • Scalbert A.
        Measuring exposure to the polyphenol metabolome in observational epidemiologic studies: Current tools and applications and their limits.
        Am J Clin Nutr. 2014; 100: 11-26
        • Rothwell J.A.
        • Knaze V.
        • Zamora-Ros R.
        Polyphenols: Dietary assessment and role in the prevention of cancers.
        Curr Opin Clin Nutr Metab Care. 2017; 20: 512-521
        • Grosso G.
        • Godos J.
        • Lamuela-Raventos R.
        • et al.
        A comprehensive meta-analysis on dietary flavonoid and lignan intake and cancer risk: Level of evidence and limitations.
        Mol Nutr Food Res. 2017; 61
        • Lei L.
        • Yang Y.
        • He H.
        • et al.
        Flavan-3-ols consumption and cancer risk: A meta-analysis of epidemiologic studies.
        Oncotarget. 2016; 7: 73573-73592
        • Russo G.I.
        • Campisi D.
        • Di Mauro M.
        • et al.
        Dietary consumption of phenolic acids and prostate cancer: A case-control study in sicily, Southern Italy.
        Molecules. 2017; 22
        • Gardeazabal I.
        • Romanos-Nanclares A.
        • Martínez-González M.A.
        • et al.
        Total polyphenol intake and breast cancer risk in the SUN cohort.
        Br J Nutr. 2019; 122: 542-551
        • Zamora-Ros R.
        • Rothwell J.A.
        • Scalbert A.
        • et al.
        Dietary intakes and food sources of phenolic acids in the European Prospective Investigation into Cancer and Nutrition (EPIC) study.
        Br J Nutr. 2013; 110: 1500-1511
        • Nagasaka R.
        • Chotimarkorn C.
        • Shafiqul I.M.
        • Hori M.
        • Ozaki H.
        • Ushio H.
        Anti-inflammatory effects of hydroxycinnamic acid derivatives.
        Biochem Biophys Res Commun. 2007; 358: 615-619
        • De P.
        • Baltas M.
        • Bedos-Belval F.
        Cinnamic acid derivatives as anticancer agents-a review.
        Curr Med Chem. 2011; 18: 1672-1703
        • Kylli P.
        • Nousiainen P.
        • Biely P.
        • Sipilä J.
        • Tenkanen M.
        • Heinonen M.
        Antioxidant potential of hydroxycinnamic acid glycoside esters.
        J Agric Food Chem. 2008; 56: 4797-4805
        • Thom E.
        The effect of chlorogenic acid enriched coffee on glucose absorption in healthy volunteers and its effect on body mass when used long-term in overweight and obese people.
        J Int Med Res. 2007; 35: 900-908
        • Carlos S.
        • De La Fuente-Arrillaga C.
        • Bes-Rastrollo M.
        • et al.
        Mediterranean diet and health outcomes in the SUN Cohort.
        Nutrients. 2018; 10: 439
        • Willett W.
        Nutritional Epidemiology.
        3rd ed. Oxford University Press, New York, NY2012
        • de la Fuente-Arrillaga C.
        • Vázquez Ruiz Z.
        • Bes-Rastrollo M.
        • Sampson L.
        • Martinez-González M.A.
        Reproducibility of an FFQ validated in Spain.
        Public Health Nutr. 2010; 13: 1364-1372
        • Martin-Moreno J.M.
        • Boyle P.
        • Gorgojo L.
        • et al.
        Development and validation of a food frequency questionnaire in Spain.
        Int J Epidemiol. 1993; 22: 512-519
        • Fernández-Ballart J.D.
        • Piñol J.L.
        • Zazpe I.
        • et al.
        Relative validity of a semi-quantitative food-frequency questionnaire in an elderly Mediterranean population of Spain.
        Br J Nutr. 2010; 103: 1808-1816
        • Neveu V.
        • Perez-Jimenez J.
        • Vos F.
        • et al.
        Phenol-Explorer: An online comprehensive database on polyphenol contents in foods.
        Database. 2010; 2010 (bap024-bap024)
        • Bognár D.A.
        Tables on weight yield of food and retention factors of food constituents for the calculation of nutrient composition of cooked foods (dishes).
        (Published 2002. Accessed December 3, 2019)
        • Rothwell J.A.
        • Medina-Remón A.
        • Pérez-Jiménez J.
        • et al.
        Effects of food processing on polyphenol contents: A systematic analysis using Phenol-Explorer data.
        Mol Nutr Food Res. 2015; 59: 160-170
        • Willet W.
        • Howe G.
        • Kushi L.
        Adjustment for total energy intake in epidemiologic studies.
        Am J Clin Nutr. 1997; 65: 1220S-1228S
        • Moreiras O.
        Tablas de Composición de Alimentos: Guía de Prácticas.
        Pirámide, Madrid2015
        • Mataix Verdú F.J.
        • Universidad de Granada, Instituto de Nutrición y Tecnología de los Alimentos
        Tabla de Composición de Alimentos.
        Universidad de Granada, Instituto de Nutrición y Tecnología de los Alimentos, Granada, Spain2009
        • Trichopoulou A.
        • Costacou T.
        • Bamia C.
        • Trichopoulos D.
        Adherence to a Mediterranean diet and survival in a Greek population.
        N Engl J Med. 2003; 348: 2599-2608
        • Martinez-Gonzalez M.A.
        • Lopez-Fontana C.
        • Varo J.J.
        • Sanchez-Villegas A.
        • Martinez J.A.
        Validation of the Spanish version of the physical activity questionnaire used in the Nurses’ Health Study and the Health Professionals’ Follow-up Study.
        Public Health Nutr. 2005; 8: 920-927
        • Bes-Rastrollo M.
        • Pérez Valdivieso J.R.
        • Sánchez-Villegas A.
        • Alonso Á.
        • Martínez-González M.Á.
        Validación del peso e índice de masa corporal auto-declarados de los participantes de una cohorte de graduados universitarios.
        Rev Esp Obes. 2005; 3: 352-358
        • Hernán M.A.
        • Hernández-Diaz S.
        • Werler M.M.
        • Mitchell A.A.
        Causal knowledge as a prerequisite for confounding evaluation: An application to birth defects epidemiology.
        Am J Epidemiol. 2002; 155: 176-184
        • Greenland S.
        • Daniel R.
        • Pearce N.
        Outcome modelling strategies in epidemiology: Traditional methods and basic alternatives.
        Int J Epidemiol. 2016; 45: 565-575
        • Royston P.
        • Lambert P.C.
        Flexible Parametric Survival Analysis Using Stata: Beyond the Cox Model.
        Stata Press, College Station, TX2011
        • Shivappa N.
        • Sandin S.
        • Lof M.
        • Hebert J.R.
        • Adami H.-O.
        • Weiderpass E.
        Prospective study of dietary inflammatory index and risk of breast cancer in Swedish women.
        Br J Cancer. 2015; 113: 1099-1103
      1. Stata Statistical Software [computer program]. Release 12. Stata Corporation LP, College Station, TX2011
        • Tresserra-Rimbau A.
        • Medina-Remón A.
        • Pérez-Jiménez J.
        • et al.
        Dietary intake and major food sources of polyphenols in a Spanish population at high cardiovascular risk: The PREDIMED study.
        Nutr Metab Cardiovasc Dis. 2013; 23: 953-959
        • Zamora-Ros R.
        • Knaze V.
        • Rothwell J.A.
        • et al.
        Dietary polyphenol intake in Europe: The European Prospective Investigation into Cancer and Nutrition (EPIC) study.
        Eur J Nutr. 2016; 55: 1359-1375
        • Vauzour D.
        • Rodriguez-Mateos A.
        • Corona G.
        • Oruna-Concha M.J.
        • Spencer J.P.E.
        Polyphenols and human health: Prevention of disease and mechanisms of action.
        Nutrients. 2010; 2: 1106-1131
        • Rocha L.D.
        • Monteiro M.C.
        • Teodoro A.J.
        Anticancer properties of hydroxycinnamic acids—A review.
        Cancer Clin Oncol. 2012; 1: p109
        • Radtke J.
        • Linseisen J.
        • Wolfram G.
        Phenolic acid intake of adults in a Bavarian subgroup of the national food consumption survey.
        Z Ernahrungswiss. 1998; 37: 190-197
        • Ovaskainen M.-L.
        • Törrönen R.
        • Koponen J.M.
        • et al.
        Dietary intake and major food sources of polyphenols in Finnish adults.
        J Nutr. 2008; 138: 562-566
        • Pérez-Jiménez J.
        • Fezeu L.
        • Touvier M.
        • et al.
        Dietary intake of 337 polyphenols in French adults.
        Am J Clin Nutr. 2011; 93: 1220-1228
        • Weng C.J.
        • Yen G.C.
        Chemopreventive effects of dietary phytochemicals against cancer invasion and metastasis: Phenolic acids, monophenol, polyphenol, and their derivatives.
        Cancer Treat Rev. 2012; 38: 76-87
        • Gorzynik-Debicka M.
        • Przychodzen P.
        • Cappello F.
        • et al.
        Potential health benefits of olive oil and plant polyphenols.
        Int J Mol Sci. 2018; 19: 686
        • Losada-Echeberría M.
        • Herranz-López M.
        • Micol V.
        • Barrajón-Catalán E.
        Polyphenols as promising drugs against main breast cancer signatures.
        Antioxidants. 2017; 6: 88
        • Mocanu M.-M.
        • Nagy P.
        • Szöllősi J.
        Chemoprevention of breast cancer by dietary polyphenols.
        Molecules. 2015; 20: 22578-22620
        • Johnston K.L.
        • Clifford M.N.
        • Morgan L.M.
        Coffee acutely modifies gastrointestinal hormone secretion and glucose tolerance in humans: Glycemic effects of chlorogenic acid and caffeine.
        Am J Clin Nutr. 2003; 78: 728-733
        • Gunter M.J.
        • Hoover D.R.
        • Yu H.
        • et al.
        Insulin, insulin-like growth factor-I, and risk of breast cancer in postmenopausal women.
        J Natl Cancer Inst. 2009; 101: 48-60
        • Garg S.K.
        Green coffee bean.
        in: Gupta R.C. Nutraceuticals: Efficacy, Safety and Toxicity. Academic Press, London2016 (653-667)
        • Nakatani N.
        • Kayano S.I.
        • Kikuzaki H.
        • Sumino K.
        • Katagiri K.
        • Mitani T.
        Identification, quantitative determination, and antioxidative activities of chlorogenic acid isomers in prune (Prunus domestica L.).
        J Agric Food Chem. 2000; 48: 5512-5516
        • Manach C.
        • Scalbert A.
        • Morand C.
        • Rémésy C.
        • Jiménez L.
        Polyphenols: Food sources and bioavailability.
        Am J Clin Nutr. 2004; 79: 727-747
        • Pérez-Jiménez J.
        • Neveu V.
        • Vos F.
        • Scalbert A.
        Identification of the 100 richest dietary sources of polyphenols: An application of the Phenol-Explorer database.
        Eur J Clin Nutr. 2010; 64: S112-S120
        • Burkholder-Cooley N.M.
        • Rajaram S.S.
        • Haddad E.H.
        • Oda K.
        • Fraser G.E.
        • Jaceldo-Siegl K.
        Validating polyphenol intake estimates from a food-frequency questionnaire by using repeated 24-h dietary recalls and a unique method-of-triads approach with 2 biomarkers.
        Am J Clin Nutr. 2017; 105: 685-694
        • Rothman K.J.
        Epidemiology: An Introduction.
        2nd ed. Oxford University Press, Oxford, UK2012

      Biography

      A. Romanos-Nanclares is a registered dietitian and PhD student, Department of Preventive Medicine and Public Health, School of Medicine, University of Navarra, Spain, and Navarra Institute for Health Research, Pamplona, Spain.

      Biography

      C. Sánchez-Quesada is a PhD, Immunology Division, Department of Health Sciences, University of Jaén, Jaén, Spain.

      Biography

      I. Gardeazábal is a Medical Doctor and PhD, Department of Preventive Medicine and Public Health, University of Navarra, Spain, and in the Department of Oncology, University of Navarra Clinic, Navarra, Spain.

      Biography

      M. A. Martínez-González is chair, Department of Preventive Medicine and Public Health, School of Medicine, University of Navarra, Navarra, Spain, Center for Physiopathology of Obesity and Nutrition, Institute of Health Carlos III, Madrid, Spain, Navarra Institute for Health Research, Pamplona, Spain, and an adjunct professor, Department of Nutrition, Harvard T. H. Chan School of Public Health, Boston, MA.

      Biography

      A. Gea is assistant professor, Department of Preventive Medicine and Public Health, School of Medicine, University of Navarra, Navarra, Spain, Center for Physiopathology of Obesity and Nutrition, Institute of Health Carlos III, Madrid, Spain, and Navarra Institute for Health Research, Pamplona, Spain.

      Biography

      E. Toledo is associate professor, Department of Preventive Medicine and Public Health, School of Medicine, University of Navarra, Navarra, Spain, Center for Physiopathology of Obesity and Nutrition, Institute of Health Carlos III, Madrid, Spain, and Navarra Institute for Health Research, Pamplona, Spain.