Top

Published in:

Open Access 01-12-2021 | Biomarkers | Research article

Adherence to the Mediterranean diet assessed by a novel dietary biomarker score and mortality in older adults: the InCHIANTI cohort study

Authors: Nicole Hidalgo-Liberona, Tomás Meroño, Raul Zamora-Ros, Montserrat Rabassa, Richard Semba, Toshiko Tanaka, Stefania Bandinelli, Luigi Ferrucci, Cristina Andres-Lacueva, Antonio Cherubini

Published in: BMC Medicine | Issue 1/2021

Abstract

Background

Dietary biomarkers may complement dietary intake assessment made by dietary questionnaires. We developed an a-posteriori dietary biomarkers score based on Mediterranean diet food groups and evaluated its association with mortality.

Methods

642 participants (56% female), aged ≥65 years, with complete data on dietary biomarkers were followed during 20 years in the InCHIANTI cohort study (Tuscany, Italy). The main outcomes were all-cause, cardiovascular, and cancer mortality. Dietary biomarkers were selected from literature and from correlation analyses with dietary intakes of Mediterranean diet food groups in the study. The baseline levels of the following dietary biomarkers were chosen: urinary total polyphenols and resveratrol metabolites, and plasma carotenoids, selenium, vitamin B12, linolenic, eicosapentaenoic and docosahexaenoic acids, and the mono-unsaturated/saturated fatty acid ratio. Associations of the Mediterranean diet score using dietary biomarkers and a validated food frequency questionnaire (FFQ) (as tertiles) with mortality were assessed through Cox regression.

Results

During the 20-year follow-up [median (Q1–Q3), 14 (8–18) years], and 435 deaths occurred (139 from cardiovascular diseases and 89 from cancer-related causes). In the fully adjusted models, the dietary biomarker-Mediterranean diet score was inversely associated with all-cause (HR_T3vs.T1 0.72; 95%CI 0.56–0.91) and cardiovascular (HR_T3vs.T1 0.60; 95%CI 0.38–0.93), but not with cancer mortality. Associations between the FFQ-Mediterranean diet score and mortality were not statistically significant.

Conclusions

A greater adherence at baseline to a Mediterranean diet assessed by a dietary biomarker score was associated with a lower risk of mortality in older adults during a 20-year follow-up. The measurement of dietary biomarkers may contribute to guide individualized dietary counseling to older people.

Trial registration

NCT01331512

Available only for authorised users

European Commission - Eurostat (2019) Ageing Europe - looking at the lives of older people in the EU. Eur Union. https://doi.org/https://doi.org/10.2785/811048

World Health Organization (2015) World report on ageing and health. World Health Organ. https://doi.org/https://doi.org/10.1007/s13398-014-0173-7.2

Wouterse B, Huisman M, Meijboom BR, Deeg DJH, Polder JJ. The effect of trends in health and longevity on health services use by older adults. BMC Health Serv Res. 2015;15(1):574. https://doi.org/10.1186/s12913-015-1239-8.CrossRefPubMedPubMedCentral

Anton SD, Cruz-Almeida Y, Singh A, Alpert J, Bensadon B, Cabrera M, Clark DJ, Ebner NC, Esser KA, Fillingim RB, Goicolea SM, Han SM, Kallas H, Johnson A, Leeuwenburgh C, Liu AC, Manini TM, Marsiske M, Moore F, Qiu P, Mankowski RT, Mardini M, McLaren C, Ranka S, Rashidi P, Saini S, Sibille KT, Someya S, Wohlgemuth S, Tucker C, Xiao R, Pahor M. Innovations in Geroscience to enhance mobility in older adults. Exp Gerontol. 2020;142:111123. https://doi.org/10.1016/j.exger.2020.111123.

Black M, Bowman M. Nutrition and healthy aging. Clin Geriatr Med. 2020;36(4):655–69. https://doi.org/10.1016/j.cger.2020.06.008.CrossRefPubMed

Capurso C, Bellanti F, Lo Buglio A, Vendemiale G. The Mediterranean diet slows down the progression of aging and helps to prevent the onset of frailty: a narrative review. Nutrients. 2019;12(1):35. https://doi.org/10.3390/nu12010035.CrossRefPubMedCentral

Bonaccio M, Di Castelnuovo A, Costanzo S, Gialluisi A, Persichillo M, Cerletti C, et al. Mediterranean diet and mortality in the elderly: a prospective cohort study and a meta-analysis. Br J Nutr. 2018;120(8):841–54. https://doi.org/10.1017/S0007114518002179.CrossRefPubMed

Trichopoulou A, Orfanos P, Norat T, Bueno-de-Mesquita B, Ocké MC, Peeters PHM, et al. Modified Mediterranean diet and survival: EPIC-elderly prospective cohort study. Br Med J. 2005;330(7498):991–5. https://doi.org/10.1136/bmj.38415.644155.8F.CrossRef

Tyrovolas S, Pounis G, Zeimbekis A, Antonopoulou M, Bountziouka V, Gotsis E, et al. Associations of energy intake and type 2 diabetes with hypertryglyceridemia in older adults living in the Mediterranean islands: The Medis study. J Nutr Elder. 2010;29(1):72–86. https://doi.org/10.1080/01639360903574668.CrossRefPubMed

10.

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(26):2599–608. https://doi.org/10.1056/NEJMoa025039.CrossRef

11.

Lassale C, Gunter MJ, Romaguera D, Peelen LM, van der Schouw YT, Beulens JWJ, et al. Diet quality scores and prediction of all-cause, cardiovascular and cancer mortality in a Pan-European Cohort study. PLoS One. 2016;11(7):e0159025. https://doi.org/10.1371/journal.pone.0159025.CrossRefPubMedPubMedCentral

12.

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(12):2918–27. https://doi.org/10.1002/ijc.27958.CrossRefPubMed

13.

Zamora-Ros R, Rabassa M, Cherubini A, Urpí-Sardà M, Bandinelli S, Ferrucci L, et al. High concentrations of a urinary biomarker of polyphenol intake are associated with decreased mortality in older adults. J Nutr. 2013;143(9):1445–50. https://doi.org/10.3945/jn.113.177121.CrossRefPubMedPubMedCentral

14.

Lelli D, Antonelli Incalzi R, Ferrucci L, Bandinelli S, Pedone C. Association between PUFA intake and serum concentration and mortality in older adults: a cohort study. Clin Nutr. 2020;39(2):510–5. https://doi.org/10.1016/j.clnu.2019.02.030.CrossRefPubMed

15.

Medina-Remón A, Barrionuevo-González A, Zamora-Ros R, Andres-Lacueva C, Estruch R, Martínez-González MÁ, et al. Rapid Folin-Ciocalteu method using microtiter 96-well plate cartridges for solid phase extraction to assess urinary total phenolic compounds, as a biomarker of total polyphenols intake. Anal Chim Acta. 2009;634(1):54–60. https://doi.org/10.1016/j.aca.2008.12.012.CrossRefPubMed

16.

Cuparencu C, Praticó G, Hemeryck LY, Sri Harsha PSC, Noerman S, Rombouts C, Xi M, Vanhaecke L, Hanhineva K, Brennan L, Dragsted LO. Biomarkers of meat and seafood intake: an extensive literature review. Genes Nutr. 2019;14:35. https://doi.org/10.1186/s12263-019-0656-4.

17.

Marklund M, Magnusdottir OK, Rosqvist F, Cloetens L, Landberg R, Kolehmainen M, et al. A dietary biomarker approach captures compliance and cardiometabolic effects of a healthy nordic diet in individuals with metabolic syndrome. J Nutr. 2014;144(10):1642–9. https://doi.org/10.3945/jn.114.193771.CrossRefPubMed

18.

Garcia-Aloy M, Hulshof PJM, Estruel-Amades S, Osté MCJ, Lankinen M, Geleijnse JM, de Goede J, Ulaszewska M, Mattivi F, Bakker SJL, Schwab U, Andres-Lacueva C. Biomarkers of food intake for nuts and vegetable oils: an extensive literature search. Genes Nutr. 2019;14:7. https://doi.org/10.1186/s12263-019-0628-8.

19.

Zheng JS, Sharp SJ, Imamura F, Chowdhury R, Gundersen TE, Steur M, Sluijs I, van der Schouw YT, Agudo A, Aune D, Barricarte A, Boeing H, Chirlaque MD, Dorronsoro M, Freisling H, el-Fatouhi D, Franks PW, Fagherazzi G, Grioni S, Gunter MJ, Kyrø C, Katzke V, Kühn T, Khaw KT, Laouali N, Masala G, Nilsson PM, Overvad K, Panico S, Papier K, Quirós JR, Rolandsson O, Redondo-Sánchez D, Ricceri F, Schulze MB, Spijkerman AMW, Tjønneland A, Tong TYN, Tumino R, Weiderpass E, Danesh J, Butterworth AS, Riboli E, Forouhi NG, Wareham NJ. Association of plasma biomarkers of fruit and vegetable intake with incident type 2 diabetes: EPIC-InterAct case-cohort study in eight European countries. BMJ. 2020;370:m2194. https://doi.org/10.1136/bmj.m2194.

20.

Li J, Guasch-Ferré M, Chung W, et al. The Mediterranean diet, plasma metabolome, and cardiovascular disease risk. Eur Heart J. 2020;41:2645–56. https://doi.org/10.1093/eurheartj/ehaa209.

21.

Ferrucci L, Bandinelli S, Benvenuti E, Di Iorio A, Macchi C, Harris TB, et al. Subsystems contributing to the decline in ability to walk: bridging the gap between epidemiology and geriatric practice in the InCHIANTI study. J Am Geriatr Soc. 2000;48(12):1618–25. https://doi.org/10.1111/j.1532-5415.2000.tb03873.x.CrossRefPubMed

22.

Lachat C, Hawwash D, Ocké MC, Berg C, Forsum E, Hörnell A, et al. Strengthening the Reporting of Observational Studies in Epidemiology—Nutritional Epidemiology (STROBE-nut): an extension of the STROBE statement. PLoS Med. 2016;13(6):e1002036. https://doi.org/10.1371/journal.pmed.1002036.CrossRefPubMedPubMedCentral

23.

Pisani P, Faggiano F, Krogh V, Palli D, Vineis P, Berrino F. Relative validity and reproducibility of a food frequency dietary questionnaire for use in the Italian EPIC centres. Int J Epidemiol. 1997;26(Suppl 1):S152–60. https://doi.org/10.1093/ije/26.suppl_1.S152.CrossRefPubMed

24.

Bartali B, Frongillo EA, Bandinelli S, Lauretani F, Semba RD, Fried LP, et al. Low nutrient intake is an essential component of frailty in older persons. J Gerontol Ser A Biol Sci Med Sci. 2006;61(6):589–93. https://doi.org/10.1093/gerona/61.6.589.CrossRef

25.

Buckland G, Agudo A, Luján L, Jakszyn P, Bueno-de-Mesquita HB, Palli D, et al. Adherence to a Mediterranean diet and risk of gastric adenocarcinoma within the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort study. Am J Clin Nutr. 2010;91(2):381–90. https://doi.org/10.3945/ajcn.2009.28209.CrossRefPubMed

26.

Lauretani F, Semba RD, Bandinelli S, Dayhoff-Brannigan M, Giacomini V, Corsi AM, et al. Low plasma carotenoids and skeletal muscle strength decline over 6 years. J Gerontol Ser A Biol Sci Med Sci. 2008;63(4):376–83. https://doi.org/10.1093/gerona/63.4.376.CrossRef

27.

Lauretani F, Semba RD, Dayhoff-Brannigan M, Corsi AM, Di Iorio A, Buiatti E, et al. Low total plasma carotenoids are independent predictors of mortality among older persons. Eur J Nutr. 2008;47(6):335–40. https://doi.org/10.1007/s00394-008-0732-9.CrossRefPubMedPubMedCentral

28.

Lauretani F, Semba RD, Bandinelli S, Ray AL, Guralnik JM, Ferrucci L. Association of low plasma selenium concentrations with poor muscle strength in older community-dwelling adults: the InCHIANTI Study. Am J Clin Nutr. 2007;86(2):347–52. https://doi.org/10.1093/ajcn/86.2.347.CrossRefPubMed

29.

Ferrucci L, Cherubini A, Bandinelli S, Bartali B, Corsi A, Lauretani F, et al. Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers. J Clin Endocrinol Metab. 2006;91(2):439–46. https://doi.org/10.1210/jc.2005-1303.CrossRefPubMed

30.

Gori AM, Sofi F, Corsi AM, Gazzini A, Sestini I, Lauretani F, et al. Predictors of vitamin B6 and folate concentrations in older persons: the InCHIANTI study. Clin Chem. 2006;52(7):1318–24. https://doi.org/10.1373/clinchem.2005.066217.CrossRefPubMedPubMedCentral

31.

Zamora-Ros R, Rabassa M, Cherubini A, Urpi-Sarda M, Llorach R, Bandinelli S, et al. Comparison of 24-h volume and creatinine-corrected total urinary polyphenol as a biomarker of total dietary polyphenols in the Invecchiare InCHIANTI study. Anal Chim Acta. 2011;704(1-2):110–5. https://doi.org/10.1016/j.aca.2011.07.035.CrossRefPubMedPubMedCentral

32.

Semba RD, Ferrucci L, Bartali B, Urpí-Sarda M, Zamora-Ros R, Sun K, et al. Resveratrol levels and all-cause mortality in older community-dwelling adults. JAMA Intern Med. 2014;174(7):1077–84. https://doi.org/10.1001/jamainternmed.2014.1582.CrossRefPubMedPubMedCentral

33.

Lauretani F, Semba RD, Bandinelli S, Dayhoff-Brannigan M, Lauretani F, Corsi AM, et al. Carotenoids as protection against disability in older persons. Rejuvenation Res. 2008;11(3):557–63. https://doi.org/10.1089/rej.2007.0581.CrossRefPubMedPubMedCentral

34.

Cherubini A, Andres-Lacueva C, Martin A, Lauretani F, Di Iorio A, Bartali B, et al. Low plasma N-3 fatty acids and dementia in older persons: The InCHIANTI study. J Gerontol Ser A Biol Sci Med Sci. 2007;62(10):1120–6. https://doi.org/10.1093/gerona/62.10.1120.CrossRef

35.

Neuhouser ML, Patterson RE, King IB, Horner NK, Lampe JW. Selected nutritional biomarkers predict diet quality. Public Health Nutr. 2003;6(7):703–9. https://doi.org/10.1079/PHN2003486.CrossRefPubMed

36.

Medina-Remón A, Tresserra-Rimbau A, Arranz S, Estruch R, Lamuela-Raventos RM. Polyphenols excreted in urine as biomarkers of total polyphenol intake. Bioanalysis. 2012;4(22):2705–13. https://doi.org/10.4155/bio.12.249.CrossRefPubMed

37.

Al-Delaimy WK, Ferrari P, Slimani N, et al. Plasma carotenoids as biomarkers of intake of fruits and vegetables: individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC). Eur J Clin Nutr. 2005;59(12):1387–96. https://doi.org/10.1038/sj.ejcn.1602252.CrossRefPubMed

38.

Lund-Blix NA, Rønningen KS, Bøås H, Tapia G, Andersen LF. Plasma phospholipid pentadecanoic acid, EPA, and DHA, and the frequency of dairy and fish product intake in young children. Food Nutr Res. 2016;60:31933. https://doi.org/10.3402/fnr.v60.31933.

39.

Zamora-Ros R, Urpí-Sardà M, Lamuela-Raventós RM, Estruch R, Martínez-González MÁ, Bulló M, et al. Resveratrol metabolites in urine as a biomarker of wine intake in free-living subjects: The PREDIMED Study. Free Radic Biol Med. 2009;46(12):1562–6. https://doi.org/10.1016/j.freeradbiomed.2008.12.023.CrossRefPubMed

40.

Obeid R, Heil SG, Verhoeven MMA, van den Heuvel EGHM, de Groot LCPGM, Eussen SJPM. Vitamin B12 intake from animal foods, biomarkers, and health aspects. Front Nutr. 2019;6:93.CrossRef

41.

Tanaka T, Shen J, Abecasis GR, Kisialiou A, Ordovas JM, Guralnik JM, et al. Genome-wide association study of plasma polyunsaturated fatty acids in the InCHIANTI study. PLoS Genet. 2009;5(1):e1000338. https://doi.org/10.1371/journal.pgen.1000338.CrossRefPubMedPubMedCentral

42.

Walter S, MacKenbach J, Vokó Z, et al. Genetic, physiological, and lifestyle predictors of mortality in the general population. Am J Public Health. 2012;102(4):e3–e10. https://doi.org/10.2105/AJPH.2011.300596.CrossRefPubMedPubMedCentral

43.

Tanaka T, Dutta A, Pilling LC, Xue L, Lunetta KL, Murabito JM, et al. Genome-wide association study of parental life span. J Gerontol Ser A Biol Sci Med Sci. 2017;72:1407–10.

44.

Elosua R, Bartali B, Ordovas JM, Corsi AM, Lauretani F, Ferrucci L. Association between physical activity, physical performance, and inflammatory biomarkers in an elderly population: the InCHIANTI study. J Gerontol Ser A Biol Sci Med Sci. 2005;60(6):760–7. https://doi.org/10.1093/gerona/60.6.760.CrossRef

45.

Fabbri E, An Y, Zoli M, Simonsick EM, Guralnik JM, Bandinelli S, et al. Aging and the burden of multimorbidity: associations with inflammatory and anabolic hormonal biomarkers. Med Sci Cite J as J Gerontol A Biol Sci Med Sci. 2015;70(1):63–70. https://doi.org/10.1093/gerona/glu127.CrossRef

46.

Harrell FE. Regression modeling strategies. Regres Model Strateg. 2015. https://doi.org/10.1007/978-3-319-19425-7.

47.

Knoops KTB, De Groot LCPGM, Kromhout D, Perrin AE, Moreiras-Varela O, Menotti A, et al. Mediterranean diet, lifestyle factors, and 10-year mortality in elderly European men and women: the HALE project. J Am Med Assoc. 2004;292(12):1433–9. https://doi.org/10.1001/jama.292.12.1433.CrossRef

48.

Zaslavsky O, Zelber-Sagi S, Hebert JR, Steck SE, Shivappa N, Tabung FK, et al. Biomarker-calibrated nutrient intake and healthy diet index associations with mortality risks among older and frail women from the Women’s Health Initiative. Am J Clin Nutr. 2017;105(6):1399–407. https://doi.org/10.3945/ajcn.116.151530.CrossRefPubMedPubMedCentral

49.

de Vries JHM, de Groot LCPGM, van Staveren WA. Dietary assessment in elderly people: experiences gained from studies in the Netherlands. Eur J Clin Nutr. 2009;63(S1):S69–74. https://doi.org/10.1038/ejcn.2008.68.CrossRefPubMed

50.

Tong TYNY, Koulman A, Griffin JL, Wareham NJ, Forouhi NG, Imamura F. A combination of metabolites predicts adherence to the Mediterranean diet pattern and its associations with insulin sensitivity and lipid homeostasis in the general population: the Fenland study United Kingdom. J Nutr. 2020;150:568–78. https://doi.org/10.1093/jn/nxz263.

51.

Picó C, Serra F, Rodríguez AM, Keijer J, Palou A. Biomarkers of Nutrition and health: new tools for new approaches. Nutrients. 2019;11:5. https://doi.org/10.3390/nu11051092.

52.

Evans C. Malnutrition in the elderly: a multifactorial failure to thrive. Perm J. 2005;9(3):38-41 https://doi.org/10.7812/tpp/05-056.

53.

Galbete C, Schwingshackl L, Schwedhelm C, Boeing H, Schulze MB. Evaluating Mediterranean diet and risk of chronic disease in cohort studies: an umbrella review of meta-analyses. Eur J Epidemiol. 2018;33(10):909–31. https://doi.org/10.1007/s10654-018-0427-3.CrossRefPubMedPubMedCentral

54.

Kabat GC, Kim M, Adams-Campbell LL, Caan BJ, Chlebowski RT, Neuhouser ML, et al. Longitudinal study of serum carotenoid, retinol, and tocopherol concentrations in relation to breast cancer risk among postmenopausal women. Am J Clin Nutr. 2009;90(1):162–9. https://doi.org/10.3945/ajcn.2009.27568.CrossRefPubMedPubMedCentral

55.

Comstock GW, Burke AE, Hoffman SC, Norkus EP, Gross M, Helzlsouer KJ. The repeatability of serum carotenoid, retinoid, and tocopherol concentrations in specimens of blood collected 15 years apart. Cancer Epidemiol. Prev. Biomarkers. 2001;10(1):65-8.

56.

Zheng J-S, Imamura F, Sharp SJ, Koulman A, Griffin JL, Mulligan AA, et al. Changes in plasma phospholipid fatty acid profiles over 13 years and correlates of change: European Prospective Investigation into Cancer and Nutrition-Norfolk Study. Am J Clin Nutr. 2019;109(6):1527–34. https://doi.org/10.1093/ajcn/nqz030.CrossRefPubMedPubMedCentral

57.

Münger LH, Garcia-Aloy M, Vázquez-Fresno R, Gille D, Rosana ARR, Passerini A, et al. Biomarker of food intake for assessing the consumption of dairy and egg products. Genes Nutr. 2018;13(1):26. https://doi.org/10.1186/s12263-018-0615-5.CrossRefPubMedPubMedCentral

58.

Brouwer-Brolsma EM, Brandl B, Buso MEC, Skurk T, Manach C. Food intake biomarkers for green leafy vegetables, bulb vegetables, and stem vegetables: a review. Genes Nutr. 2020;15(1):7. https://doi.org/10.1186/s12263-020-00667-z.

59.

Ulaszewska M, Vázquez-Manjarrez N, Garcia-Aloy M, Llorach R, Mattivi F, Dragsted LO, et al. Food intake biomarkers for apple, pear, and stone fruit. Genes Nutr. 2018;13(1):29. https://doi.org/10.1186/s12263-018-0620-8.CrossRefPubMedPubMedCentral

Title: Adherence to the Mediterranean diet assessed by a novel dietary biomarker score and mortality in older adults: the InCHIANTI cohort study
Authors: Nicole Hidalgo-Liberona
Tomás Meroño
Raul Zamora-Ros
Montserrat Rabassa
Richard Semba
Toshiko Tanaka
Stefania Bandinelli
Luigi Ferrucci
Cristina Andres-Lacueva
Antonio Cherubini
Publication date: 01-12-2021
Publisher: BioMed Central
Keyword: Biomarkers
Published in: BMC Medicine / Issue 1/2021
Electronic ISSN: 1741-7015
DOI: https://doi.org/10.1186/s12916-021-02154-7

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Adherence to the Mediterranean diet assessed by a novel dietary biomarker score and mortality in older adults: the InCHIANTI cohort study

Abstract

Background

Methods

Results

Conclusions

Trial registration

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Trial registration

Please log in to get access to this content

Other articles of this Issue 1/2021

Can we achieve better recruitment by providing better information? Meta-analysis of ‘studies within a trial’ (SWATs) of optimised participant information sheets

Differential effect of pre-pregnancy low BMI on fetal macrosomia: a population-based cohort study

Targeting body composition in an older population: do changes in movement behaviours matter? Longitudinal analyses in the PREDIMED-Plus trial

Association of healthy lifestyle score with all-cause mortality and life expectancy: a city-wide prospective cohort study of cancer survivors

The importance of transdiagnostic symptom level assessment to understanding prognosis for depressed adults: analysis of data from six randomised control trials

Allergy-related diseases in childhood and risk for abdominal pain-related functional gastrointestinal disorders at 16 years—a birth cohort study