Top

Published in:

Open Access 01-12-2023 | Research article

Change in habitual intakes of flavonoid-rich foods and mortality in US males and females

Authors: Nicola P. Bondonno, Yan Lydia Liu, Yan Zheng, Kerry Ivey, Walter C. Willett, Meir J. Stampfer, Eric B. Rimm, Aedín Cassidy

Published in: BMC Medicine | Issue 1/2023

Abstract

Background

Higher baseline intakes of flavonoid-rich foods and beverages are associated with a lower risk of chronic disease and mortality in observational studies. However, associations between changes in intakes and mortality remain unclear. We aimed to evaluate associations between 8-year changes in intakes of (1) individual flavonoid-rich foods and (2) a composite measure (termed the ‘flavodiet’) of foods and beverages that are known to be main contributors to flavonoid intake and subsequent total and cause-specific mortality.

Methods

We evaluated associations between 8-year changes in intakes of (1) individual flavonoid-rich foods and (2) a novel ‘flavodiet’ score and total and cause-specific mortality. We included 55,786 females from the Nurses’ Health Study (NHS) and 29,800 males from the Health Professionals Follow-up Study (HPFS), without chronic disease at baseline in our analyses. Using multivariable-adjusted Cox proportional hazard models, we examined associations of 8-year changes in intakes of (1) flavonoid-rich foods and (2) the flavodiet score with subsequent 2-year lagged 6-year risk of mortality adjusting for baseline intakes. Data were pooled using fixed-effects meta-analyses.

Results

We documented 15,293 deaths in the NHS and 8988 deaths in HPFS between 1986 and 2018. For blueberries, red wine and peppers, a 5%, 4% and 9% lower risk of mortality, respectively, was seen for each 3.5 servings/week increase in intakes while for tea, a 3% lower risk was seen for each 7 servings/week increase [Pooled HR (95% CI) for blueberries; 0.95 (0.91, 0.99); red wine: 0.96 (0.93, 0.99); peppers: 0.91 (0.88, 0.95); and tea: 0.97 (0.95, 0.98)]. Conversely, a 3.5 servings/week increase in intakes of onions and grapefruit plus grapefruit juice was associated with a 5% and 6% higher risk of total mortality, respectively. An increase of 3 servings per day in the flavodiet score was associated with an 8% lower risk of total mortality [Pooled HR: 0.92 (0.89, 0.96)], and a 13% lower risk of neurological mortality [Pooled HR: 0.87 (0.79, 0.97)], after multivariable adjustments.

Conclusions

Encouraging an increased intake of specific flavonoid-rich foods and beverages, namely tea, blueberries, red wine, and peppers, even in middle age, may lower early mortality risk.

Available only for authorised users

Bondonno NP, Dalgaard F, Kyrø C, Murray K, Bondonno CP, Lewis JR, et al. Flavonoid intake is associated with lower mortality in the Danish Diet Cancer and Health Cohort. Nat Commun. 2019;10(1):1–10.CrossRef

Bertoia ML, Mukamal KJ, Cahill LE, Hou T, Ludwig DS, Mozaffarian D, et al. Changes in intake of fruits and vegetables and weight change in United States men and women followed for up to 24 years: analysis from three prospective cohort studies. PLoS Med. 2015;12(9):e1001878.PubMedPubMedCentralCrossRef

Raman G, Avendano EE, Chen S, Wang J, Matson J, Gayer B, et al. Dietary intakes of flavan-3-ols and cardiometabolic health: systematic review and meta-analysis of randomized trials and prospective cohort studies. Am J Clin Nutr. 2019;110(5):1067–78.PubMedPubMedCentralCrossRef

Ivey KL, Jensen MK, Hodgson JM, Eliassen AH, Cassidy A, Rimm EB. Association of flavonoid-rich foods and flavonoids with risk of all-cause mortality. Br J Nutr. 2017;117(10):1470–7.PubMedPubMedCentralCrossRef

Parmenter BH, Croft KD, Hodgson JM, Dalgaard F, Bondonno CP, Lewis JR, et al. An overview and update on the epidemiology of flavonoid intake and cardiovascular disease risk. Food Funct. 2020;11(8):6777–806.PubMedCrossRef

Williamson G, Kay CD, Crozier A. The bioavailability, transport, and bioactivity of dietary flavonoids: a review from a historical perspective. Compr Rev Food Sci Food Saf. 2018;17(5):1054–112.PubMedCrossRef

Willet W, Buzzard I. Foods and Nutrients. Monogr Epidemiol Biostat. 1998;1(30):18–32.

Wilson MM, Reedy J, Krebs-Smith SM. Dietetics. American diet quality: where it is, where it is heading, and what it could be. J Acad Nutr. 2016;116(2):302–10.CrossRef

10.

Wang DD, Li Y, Bhupathiraju SN, Rosner BA, Sun Q, Giovannucci EL, et al. Fruit and vegetable intake and mortality: results from 2 prospective cohort studies of US men and women and a meta-analysis of 26 cohort studies. Circulation. 2021;143(17):1642–54.PubMedPubMedCentralCrossRef

11.

Kim K, Vance TM, Chun O. Estimated intake and major food sources of flavonoids among US adults: changes between 1999–2002 and 2007–2010 in NHANES. Eur J Nutr. 2016;55(2):833–43.PubMedCrossRef

12.

McCullough ML, Peterson JJ, Patel R, Jacques PF, Shah R, Dwyer JT. Flavonoid intake and cardiovascular disease mortality in a prospective cohort of US adults. Am J Clin Nutr. 2012;95(2):454–64.PubMedPubMedCentralCrossRef

13.

Vogiatzoglou A, Mulligan AA, Lentjes MA, Luben RN, Spencer JP, Schroeter H, et al. Flavonoid intake in European adults (18 to 64 years). PLoS ONE. 2015;10(5): e0128132.PubMedPubMedCentralCrossRef

14.

Zamora-Ros R, Knaze V, Rothwell JA, Hémon B, Moskal A, Overvad K, et al. Dietary polyphenol intake in Europe: the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Nutr. 2016;55(4):1359–75.PubMedCrossRef

15.

Bondonno NP, Lewis JR, Blekkenhorst LC, Bondonno CP, Shin JH, Croft KD, et al. Association of flavonoids and flavonoid-rich foods with all-cause mortality: The Blue Mountains Eye Study. Clin Nutr. 2020;39(1):141–50.PubMedCrossRef

16.

Bertoia ML, Rimm EB, Mukamal KJ, Hu FB, Willett WC, Cassidy A. Dietary flavonoid intake and weight maintenance: three prospective cohorts of 124 086 US men and women followed for up to 24 years. BMJ. 2016;352:i17.

17.

Colditz GA, Manson JE, Hankinson SE. The Nurses’ Health Study: 20-year contribution to the understanding of health among women. J Women’s Health. 1997;6(1):49–62.CrossRef

18.

Rimm EB, Giovannucci EL, Willett WC, Colditz GA, Ascherio A, Rosner B, et al. Prospective study of alcohol consumption and risk of coronary disease in men. Lancet. 1991;338(8765):464–8.PubMedCrossRef

19.

Cassidy A, Rimm EB, O’Reilly ÉJ, Logroscino G, Kay C, Chiuve SE, et al. Dietary flavonoids and risk of stroke in women. Stroke. 2012;43(4):946–51.PubMedPubMedCentralCrossRef

20.

Al-Shaar L, Yuan C, Rosner B, Dean SB, Ivey KL, Clowry CM, et al. Reproducibility and validity of a semiquantitative food frequency questionnaire in men assessed by multiple methods. Am J Epidemiol. 2021;190(6):1122–32.PubMedCrossRef

21.

Yuan C, Spiegelman D, Rimm EB, Rosner BA, Stampfer MJ, Barnett JB, et al. Validity of a dietary questionnaire assessed by comparison with multiple weighed dietary records or 24-hour recalls. Am J Epidemiol. 2017;185(7):570–84.PubMedPubMedCentralCrossRef

22.

Salvini S, Hunter DJ, Sampson L, Stampfer MJ, Colditz GA, Rosner B, et al. Food-based validation of a dietary questionnaire: the effects of week-to-week variation in food consumption. Int J Epidemiol. 1989;18(4):858–67.PubMedCrossRef

23.

Feskanich D, Rimm EB, Giovannucci EL, Colditz GA, Stampfer MJ, Litin LB, et al. Reproducibility and validity of food intake measurements from a semiquantitative food frequency questionnaire. J Am Diet Assoc. 1993;93(7):790–6.PubMedCrossRef

24.

Rich-Edwards JW, Corsano KA, Stampfer MJ. Test of the national death index and equifax nationwide death search. Am J Epidemiol. 1994;140(11):1016–9.PubMedCrossRef

25.

Sun Q, Townsend MK, Okereke OI, Franco OH, Hu FB, Grodstein F. Physical activity at midlife in relation to successful survival in women at age 70 years or older. Arch Intern Med. 2010;170(2):194–201.PubMedPubMedCentralCrossRef

26.

Zheng Y, Li Y, Satija A, Pan A, Sotos-Prieto M, Rimm E, et al. Association of changes in red meat consumption with total and cause specific mortality among US women and men: two prospective cohort studies. BMJ. 2019;365:l2110.

27.

Bondonno NP, Bondonno CP, Ward NC, Hodgson JM, Croft KD. The cardiovascular health benefits of apples: Whole fruit vs. isolated compounds. Trends Food Sci Technol. 2017;69:243–56.CrossRef

28.

Wojcicki JM, Heyman MB. Reducing childhood obesity by eliminating 100% fruit juice. Am J Public Health. 2012;102(9):1630–3.PubMedPubMedCentralCrossRef

29.

Genser D. Food and drug interaction: consequences for the nutrition/health status. Ann Nutr Metab. 2008;52(Suppl. 1):29–32.PubMedCrossRef

30.

Chung M, Zhao N, Wang D, Shams-White M, Karlsen M, Cassidy A, et al. Dose–response relation between tea consumption and risk of cardiovascular disease and all-cause mortality: a systematic review and meta-analysis of population-based studies. Adv Nutr. 2020;11(4):790–814.PubMedPubMedCentralCrossRef

31.

Eleftheriou D, Benetou V, Trichopoulou A, La Vecchia C, Bamia C. Mediterranean diet and its components in relation to all-cause mortality: meta-analysis. Brit J Nutr. 2018;120(10):1081–97.PubMedCrossRef

32.

Haseeb S, Alexander B, Baranchuk A. Wine and cardiovascular health: a comprehensive review. Circulation. 2017;136(15):1434–48.PubMedCrossRef

33.

Rehm J, Mathers C, Popova S, Thavorncharoensap M, Teerawattananon Y, Patra J. Global burden of disease and injury and economic cost attributable to alcohol use and alcohol-use disorders. Lancet. 2009;373(9682):2223–33.PubMedCrossRef

34.

González R, Ballester I, López-Posadas R, Suárez M, Zarzuelo A, Martinez-Augustin O, et al. Effects of flavonoids and other polyphenols on inflammation. Crit Rev Food Sci Nutr. 2011;51(4):331–62.PubMedCrossRef

35.

Gomes A, Fernandes E, Lima JL, Mira L, Corvo ML. Molecular mechanisms of anti-inflammatory activity mediated by flavonoids. Curr Med Chem. 2008;15(16):1586–605.PubMedCrossRef

36.

Landberg R, Sun Q, Rimm EB, Cassidy A, Scalbert A, Mantzoros CS, et al. Selected dietary flavonoids are associated with markers of inflammation and endothelial dysfunction in US women. J Nutr. 2011;141(4):618–25.PubMedPubMedCentralCrossRef

37.

Cassidy A, Rogers G, Peterson JJ, Dwyer JT, Lin H, Jacques PF. Higher dietary anthocyanin and flavonol intakes are associated with anti-inflammatory effects in a population of US adults. Am J Clin Nutr. 2015;102(1):172–81.PubMedPubMedCentralCrossRef

38.

Mehta AJ, Cassidy A, Litonjua AA, Sparrow D, Vokonas P, Schwartz J. Dietary anthocyanin intake and age-related decline in lung function: longitudinal findings from the VA Normative Aging Study–3. Am J Clin Nutr. 2016;103(2):542–50.PubMedPubMedCentralCrossRef

39.

Garcia-Larsen V, Thawer N, Charles D, Cassidy A, Van Zele T, Thilsing T, et al. Dietary intake of flavonoids and ventilatory function in European adults: A GA2LEN study. Nutrients. 2018;10(1):95.PubMedPubMedCentralCrossRef

40.

Bondonno NP, Parmenter BH, Dalgaard F, Murray K, Rasmussen DB, Kyrø C, et al. Flavonoid intakes inversely associate with COPD in smokers. Eur Respir J. 2022;60(2):2102604.

41.

Ayaz M, Sadiq A, Junaid M, Ullah F, Ovais M, Ullah I, et al. Flavonoids as prospective neuroprotectants and their therapeutic propensity in aging associated neurological disorders. Front Aging Neurosci. 2019;11:155.PubMedPubMedCentralCrossRef

42.

de Andrade Teles RB, Diniz TC, Costa Pinto TC, de Oliveira Júnior RG, Gama e Silva M, de Lavor ÉM, et al. Flavonoids as therapeutic agents in Alzheimer’s and Parkinson’s diseases: a systematic review of preclinical evidences. Oxid Med Cell Longev. 2018;2018:7043213.

43.

Bondonno CP, Bondonno NP, Dalgaard F, Murray K, Gardener SL, Martins RN, et al. Flavonoid intake and incident dementia in the Danish Diet, Cancer, and Health cohort. Alzheimer’s Dement: Transl Res Clin Interv. 2021;7(1): e12175.

44.

Gao X, Cassidy A, Schwarzschild M, Rimm EB, Ascherio A. Habitual intake of dietary flavonoids and risk of Parkinson disease. Neurology. 2012;78(15):1138–45.PubMedPubMedCentralCrossRef

45.

Shishtar E, Rogers GT, Blumberg JB, Au R, Jacques PF. Long-term dietary flavonoid intake and risk of Alzheimer disease and related dementias in the Framingham Offspring Cohort. Am J Clin Nutr. 2020;112(2):343–53.PubMedPubMedCentralCrossRef

46.

Holland TM, Agarwal P, Wang Y, Leurgans SE, Bennett DA, Booth SL, et al. Dietary flavonols and risk of Alzheimer dementia. Neurology. 2020;94(16):e1749–56.PubMedPubMedCentralCrossRef

47.

Gao S, Nguyen JT, Hendrie HC, Unverzagt FW, Hake A, Smith-Gamble V, et al. Accelerated weight loss and incident dementia in an elderly African-American cohort. J Am Geriatr Soc. 2011;59(1):18–25.PubMedCrossRef

48.

Fávaro-Moreira NC, Krausch-Hofmann S, Matthys C, Vereecken C, Vanhauwaert E, Declercq A, et al. Risk factors for malnutrition in older adults: a systematic review of the literature based on longitudinal data. Adv Nutr. 2016;7(3):507–22.PubMedPubMedCentralCrossRef

49.

Kai K, Hashimoto M, Amano K, Tanaka H, Fukuhara R, Ikeda M. Relationship between eating disturbance and dementia severity in patients with Alzheimer’s disease. PLoS ONE. 2015;10(8):e0133666.PubMedPubMedCentralCrossRef

50.

Perez-Jimenez 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(8):4959–69.PubMedCrossRef

51.

Bao Y, Bertoia ML, Lenart EB, Stampfer MJ, Willett WC, Speizer FE, et al. Origin, methods, and evolution of the three Nurses’ Health Studies. Am J Public Health. 2016;106(9):1573–81.PubMedPubMedCentralCrossRef

Title: Change in habitual intakes of flavonoid-rich foods and mortality in US males and females
Authors: Nicola P. Bondonno
Yan Lydia Liu
Yan Zheng
Kerry Ivey
Walter C. Willett
Meir J. Stampfer
Eric B. Rimm
Aedín Cassidy
Publication date: 01-12-2023
Publisher: BioMed Central
Published in: BMC Medicine / Issue 1/2023
Electronic ISSN: 1741-7015
DOI: https://doi.org/10.1186/s12916-023-02873-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Change in habitual intakes of flavonoid-rich foods and mortality in US males and females

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2023

Mediterranean diet adherence is associated with lower dementia risk, independent of genetic predisposition: findings from the UK Biobank prospective cohort study

Early-life exposure to the Great Chinese Famine and gut microbiome disruption across adulthood for type 2 diabetes: three population-based cohort studies

First-in-human, double-blind, randomized phase 1b study of peptide immunotherapy IMCY-0098 in new-onset type 1 diabetes

Impact of high-power short-duration atrial fibrillation ablation technique on the incidence of silent cerebral embolism: a prospective randomized controlled study

Maternal obesity and programming of metabolic syndrome in the offspring: searching for mechanisms in the adipocyte progenitor pool

Correction: Dynamic monitoring of cerebrospinal fluid circulating tumor DNA to identify unique genetic profiles of brain metastatic tumors and better predict intracranial tumor responses in non-small cell lung cancer patients with brain metastases: a prospective cohort study (GASTO 1028)