Journal of Alzheimer’s Disease 29 (2012) 1–10 Polyphenol-Rich Foods in the Mediterranean Diet are Associated with Better Cognitive Cinta Valls-Pedreta,b, Rosa Maria Lamuela-Ravent´osb,c,d, Alexander Medina-Rem´onb,c,d, Melibea Quintanaa, Dolores Corellab,e, Xavier Pint´od,f , Miguel ´ Ramon Estruchb,h and Emilio Rosa,b,∗a Lipid Clinic, Endocrinology and Nutrition Service, Institut d’Investigacions Biom`ediques August Pi i Sunyer (IDIBAPS), Hospital Cl´ınic, Barcelona, Spainb CIBER Fisiopatolog´ıa de la Obesidad y Nutrici´on (CIBERobn), Instituto de Salud Carlos III (ISCIII), Spain Nutrition and Food Science Department, XaRTA, INSA, Pharmacy School, University of Barcelona, Barcelona, RETIC RD06/0045, Instituto de Salud Carlos III (ISCIII), Spain Department of Preventive Medicine and Public Health, School of Medicine, University of Valencia, Valencia, Spain Unitat de L´ıpids i Risc Vascular, Servei de Medicina Interna, Hospital Universitari de Bellvitge, Barcelona, Spain Department of Preventive Medicine and Public Health, School of Medicine, University of Navarra, Pamplona, Department of Internal Medicine, IDIBAPS, Hospital Cl´ınic, Barcelona, Spain Handling Associate Editor: Vincenza Frisardi Abstract. Brain oxidative processes play a major role in age-related cognitive decline, thus consumption of antioxidant-rich
foods might help preserve cognition. Our aim was to assess whether consumption of antioxidant-rich foods in the Mediterranean diet relates to cognitive function in the elderly. In asymptomatic subjects at high cardiovascular risk (n = 447; 52% women; age 55–80 y) enrolled in the PREDIMED study, a primary prevention dietary-intervention trial, we assessed food intake and cardiovascular risk profile, determined apolipoprotein E genotype, and used neuropsychological tests to evaluate cognitive function. We also measured urinary polyphenols as an objective biomarker of intake. Associations between energy-adjusted food and cognitive scores were assessed by multiple linear regression models adjusted for potential confounders. Consumption of some foods was independently related to better cognitive function. The specific associations[regression coefficients (95% confidence intervals)] were: total olive oil with immediate verbal memory [0.755 (0.151–1.358)];virgin olive oil and coffee with delayed verbal memory [0.163 (0.010–0.316) and 0.294 (0.055–0.534), respectively]; walnuts with working memory [1.191 (0.061–2.322)]; and wine with Mini-Mental State Examination scores [0.252 (0.006–0.496)]. Urinary polyphenols were associated with better scores in immediate verbal memory [1.208 (0.236–2.180)]. Increased consumption of ∗Correspondence to: Emilio Ros, Lipid Clinic, Endocrinology and Nutrition Service, Hospital Cl´ınic. Villarroel 170, 08036Barcelona, Spain. Tel.: +34 932279383; Fax: +34 934537829;E-mail: ISSN 1387-2877/12/$27.50 2012 – IOS Press and the authors. All rights reserved C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging antioxidant-rich foods in general and of polyphenols in particular is associated with better cognitive performance in elderly subjects at high cardiovascular risk. The results reinforce the notion that Mediterranean diet components might counteract Keywords: Aging, coffee, cognition, Mediterranean diet, nutrition, polyphenols, olive oil, walnuts, wine INTRODUCTION
adherence to a Mediterranean-type diet is associated with a reduced incidence of coronary heart disease Increased lifespan in developed countries has (CHD) [13–15]. Consistently, epidemiological studies resulted in a greatly raised frequency of diseases point to a reduction in the incidence of and mortality related to aging, such as cardiovascular and neurode- from cardiovascular diseases [13, 15, 16] and cancer, generative disorders, including Alzheimer’s disease which results in increased longevity [16]. Importantly, (AD), the most common type of dementia [1]. AD as recently reviewed [17], increasing compliance with is characterized by cognitive deterioration with a Mediterranean-type diets has also been associated with progressive impairment of activities of daily living.
slower cognitive decline [18], a reduction in the inci- Cognitive changes, however, are not particular to dence of MCI [19], neurodegenerative disorders such severe neurodegenerative diseases like AD, as the as Parkinson’s disease [20] and AD [21, 22], and mor- aging process naturally entails normal age-associated cognitive decline. The cognitive functions that are most Oxidative stress and ensuing inflammation are frequently affected with aging are memory, especially believed to play major roles in the pathogenesis of codification, recall, and working memory, and execu- age-related diseases, including cognitive impairment tive functions that imply information processing speed, and AD. They also are ideal targets for nutritional inter- divided attention, and planning [2].
vention with antioxidants, for which the Mediterranean Factors recognized to aid in maintaining cognitive diet is particularly well suited [25]. Therefore, we eval- performance include years of schooling, professional uated in a cross-sectional study whether consumption achievement, social engagement, and physical activ- of antioxidant-rich foods from the Mediterranean diet ity [3]. Such factors are encompassed in the concept was associated with better cognitive performance in a of cognitive reserve, described as the brain’s capacity cohort of elderly persons at high risk for CHD living to compensate for neuropathological damage in brain in Spain, a Mediterranean country. In addition, since aging, making clinical symptoms unobtrusive or even there is evidence that consumption of flavonoids, a imperceptible [4]. An appealing link hypothesized in subclass of polyphenols, positively relates to cogni- recent years is the association between lifestyle habits, tive function [26], we complemented dietary data with particularly food patterns, and cognitive reserve [3, urinary polyphenol excretion, an objective biomarker 5]. Epidemiological studies suggest that foods such as fruits, vegetables, fish, and wine and nutrients such as polyunsaturated fatty acids, E and B-vitamins, and antioxidants might protect from age-related cognitive decline, mild cognitive impairment (MCI) and AD Participants and design of the study cohort of the PREDIMED (PREvenci´on con DIeta MEDiterr´anea) study, a clinical trial in asymp- among food constituents, Uncorrected Author Proof tomatic persons at high cardiovascular risk testing health [11, 12]. One such pattern is the traditional the Mediterranean diet for outcomes on cardio- Mediterranean diet, a reputed model of healthy eat- ing that is characterized by a high consumption of ISRCTN35739639). The design of the PREDIMED foods and nutrients presumed to be healthy for the study has been described in detail elsewhere [27]. Can- brain, such as vegetables, fruits, fish, unsaturated didates were community-dwelling men aged 55–80 fatty acids, and diverse antioxidants, with moderate years and women aged 60–80 years, without prior car- intake of alcoholic beverages, mostly wine [13]. Both diovascular disease but having a prior diagnosis of prospective and clinical studies report that greater diabetes or at least three cardiovascular risk factors, C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging namely smoking, hypertension, dyslipidemia, over- [33], severe cognitive impairment, defined by a score weight (body mass index (BMI) ≥25 kg/m2), and <25 in the Mini-Mental State Examination (MMSE) family history of premature cardiovascular disease [34], illiteracy, or difficulty in expression or compre- (≥55 years in men and ≥60 years in women). Other exclusion criteria were any severe chronic illness, alco- hol or drug abuse, or BMI ≥40 kg/m2. Participants fulfilling inclusion criteria and not meeting exclu- sion criteria provided informed consent to a protocol An experienced neuropsychologist who was blinded approved by the local review board and underwent to the subjects’ diet and cardiovascular risk factors various tests, including venipuncture to obtain fasting conducted the cognitive examination. The instruments blood and collection of a spot urine sample.
used were the MMSE to assess global cognitive Anthropometric and blood pressure measurements function [34]; the Rey auditory verbal learning test were performed by standard methods, as previously (RAVLT) to rate immediate (sum of words recalled described [27]. Smoking status was categorized into on the five learning trials) and delayed episodic ver- never, current or past smoking according to self- bal memory [35]; the verbal paired associates test, a reports. Physical activity was assessed with the subtest of Wechsler Memory Scale (WMS) [36], to validated Spanish version of the Minnesota question- evaluate episodic memory performance; the semantic naire and expressed in minutes at a given metabolic verbal fluency test [37]; the digit span test of the Wech- equivalent (MET-min) per day [28]. Dietary data sler Adult Intelligence Scale (WAIS) [38] to assess related to self-selected food intake during the previ- immediate memory (direct digits) and working mem- ous year were collected during a face-to-face interview ory (reverse order digits); and the Color Trail Test (part with a single trained dietitian using a validated 137- I and II) [39] to measure executive function, including item food-frequency questionnaire (FFQ) [29] and attention, visual-motor speed, and cognitive flexibility.
converted to daily intakes. Energy and nutrient intake were calculated from Spanish food composition tables.
The apolipoprotein E (APOE) genotype was deter- mined by using the method of Hixson and Vernier We fitted multiple linear regression models to assess [30]. High-sensitivity C-reactive protein (CRP) was independent associations of demographic, clinical, and measured using an immunoturbidimetric technique.
dietary variables and urinary polyphenol excretion Total polyphenols in spot urine samples were deter- with neuropsychological test scores. In the first model, mined with the Folin-Ciocalteu assay after solid phase with cognitive test scores as dependent variables, we extraction, together with the creatinine concentra- introduced the energy-adjusted intakes of various food tion, as described [31]. Total polyphenol excretion groups (cereals, vegetables, fruits, legumes, nuts, meat was expressed as mg of gallic acid equivalents and meat products, seafood, olive oil, alcohol, and cof- (GAE)/g of creatinine. Urinary total polyphenol excre- fee) as independent variables. In the second model we tion expressed by 24-h volume is a better biomarker adjusted for age, gender, education years, BMI, current of polyphenol dietary intake than expressed by uri- smoking, physical activity, APOE genotype, diabetes, nary creatinine normalization. However, when total hypertension and hyperlipidemia, and the food groups volume in 24-h is not available, creatinine-corrected that were significantly associated with test scores in the urinary total polyphenol excretion may also be a suit- first model as potential confounders. Because in addi- tion to questions on intake of total alcohol, olive oil, and nuts, the FFQ used in the study contains specific questions on intake of wine, virgin olive oil (VOO), and walnuts, we constructed additional models where recruiting centre located at Hospital Cl´ınic (Barcelona, alcohol, olive oil, and nut consumption were replaced Catalonia, Spain) were asked to submit to neuropsy- by wine and other alcoholic beverages, VOO and chological testing to assess cognitive function. During common olive oil, and walnuts and other nuts, respec- the screening visit, participants were asked about edu- tively. In a further model, we entered as independent cation years and information about exclusion criteria variable urinary polyphenol excretion alone, to avoid specific for this substudy was sought, namely depres- collinearity with other antioxidant-rich food groups, sion, as assessed by the Hamilton Depression Rating with adjustment for the same variables plus total energy Scale (participants with a score >13 were excluded) intake. Finally, the logarithmical transformed values C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging of urinary polyphenol excretion and serum CRP were Socio-demographic and anthropometric characteristics, physical entered in a partial correlation adjusted by gender, age activity, cardiovascular risk factors and APOE genotype of the study and BMI. p values <0.05 were considered significant.
SPSS software, version 16.0 (SPSS Inc., Chicago, IL) Figure 1 shows the flow of participants. By study design, there was a high prevalence of cardiovascular risk factors in the 447 participants available for analysis As shown in Table 2, the self-selected participant’s dietary habits reasonably conformed to the traditional Mediterranean food pattern in several aspects, as they recorded high intakes of cereals, vegetables, fruits, fish, Antihypertensive medication, n (%) and olive oil and moderate intakes of legumes, nuts, and wine. They deviated from the traditional Mediter- ranean diet, however, because of high intakes of meat and dairy products. The extreme ranges underscore the high between-subject variability of energy and food *Median. Sum of E4/3 and E4/4 genotypes (E2/4 excluded).
intake and urinary polyphenol excretion.
GAE/g Cr, gallic acid equivalents (GAE)/g of creatinine. Abbre- viations: MET-min, minutes at a given metabolic equivalent level(units of energy expenditure in physical activity, 1 MET-min roughly equivalent to 1 Kcal); CVD, cardiovascular disease; APOE,apolipoprotein E.
Various clinical, demographic and dietary variables were independently associated with the outcomes of neuropsychological tests by multiple linear regression Daily intake of energy and food groups of the study population analyses after adjustment for various confounders. The fully adjusted associations are shown in Table 3. Older age, diabetes, and hypertension were associated with lower MMSE scores, while higher education years and higher wine intake were associated with better perfor- mance. In the immediate recall of RAVLT, older age and cereal intake were associated with lower scores.
Conversely, higher education years, the female gen- der, and higher intake of total olive oil were associated with immediate verbal memory. Intake of coffee and C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging Independent associations of cognitive test scores with food intake by multiple linear regression Cognitive test scores are the dependent variables. The independent variables listed are those showing p < 0.05 after regression analyses.
*␤: Standardized regression coefficient. Abbreviations: MMSE, Mini Mental State Examination; RAVLT, Rey Auditory VerbalLearning Test; MET-min, minutes at a given metabolic equivalent level. Variables allowed into the models were gender, age, education,body mass index, smoking, APOE ␧4 allele, energy expenditure in physical activity, diabetes, hypertension, and hyperlipidemia.
VOO, higher education years, and the female gen- urinary polyphenol excretion and CRP (r = −0.102, der were associated with better performance in the delayed recall of RAVLT, while older age, hyperten- sion, and intake of cereals and meat were associated with lower scores. Total olive oil intake was also DISCUSSION
independently associated with the delayed recall of RAVLT (regression coefficient 0.36, p = 0.001), but In this cross-sectional evaluation of dietary habits only data on VOO is shown in Table 3 because of and cognitive function in older persons at high car- the novelty of the finding. The consumption of wal- diovascular risk living in a Mediterranean country, nuts was also associated with better working memory, higher intakes of both total olive oil and the virgin as assessed by the reverse digit span test of the WAIS variety of olive oil, coffee, walnuts, and wine were associated with better memory function and global Total urinary polyphenol excretion was significantly cognition. The magnitude of these associations was variable and they were present in some but not in all tests of cognitive function, but were independent of known cognition-related confounders and consump- tion of other food groups. The findings on VOO der and higher education years (directly) and age and walnuts, two foods with high antioxidant capac- and diabetes (inversely) also related independently ity [40, 41], are novel. Another novel finding is the to RALVT scores. Figure 2 shows that there was a independent association of total urinary polyphenol dose-relationship between urinary polyphenols and excretion, an objective biomarker of polyphenol-rich enhancement of the RAVLT score. Moreover, after food intake, with human memory function. Taken adjusting by gender, age, and BMI, we found a together, these results suggest that antioxidants in significant albeit weak inverse correlation between the usual diet might counteract age-related cognitive the logarithmically transformed values of total C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging Independent associations of cognitive test scores with urinary polyphenols excretion by multiple linear regression analysis Cognitive test scores are the dependent variables. The independent variables listed are those showing P values close to <0.05 after regressionanalyses. *␤: Standardized regression coefficient. Abbreviations: RAVLT, Rey Auditory Verbal Learning Test; GAE/g Cr, gallic acid equivalents/gof creatinine. Variables allowed in the models were gender, age, education, body mass index, energy intake (Kcal/day), smoking, APOE ␧4allele, energy expenditure in physical activity, diabetes, hypertension, and hyperlipidemia.
proportions of bioactive micronutrients, such as phy- tosterols, vitamin E, and phenolic compounds [40].
Because of a lower cost, common olive oil (a mix- ture of refined oil with a small proportion of VOO) is widely used in Spain in the kitchen and at the table, while VOO, which is obtained by cold pressing of the ripe fruit and is much richer in minor but bioactive com- ponents, has a more restricted consumption, as shown in our study group (Table 2). Greater consumption of VOO in the Mediterranean diet has been associated with various health benefits [40]. Few epidemiologi- cal studies have related consumption of MUFA with cognitive function. MUFA is contained in other foods, for example beef, besides olive oil. This heterogene- ity in the dietary sources of MUFA might explain why some results are inconsistent [42–46]. Recently, in line with our results, a weak association of total olive oil intake with a reduced risk of cognitive impairment was reported in a large French cohort [47].
We found that increasing consumption of walnuts, but not of other nuts, was associated with better work- ing memory scores. Interestingly, walnuts are among the foods with highest antioxidant capacity, by far surpassing other nuts [48]. They are also the whole food richest in ␣-linolenic acid, the vegetable n-3 fatty acid [41]. Consistent evidence from prospective studies suggests that frequent nut intake relates to lower CHD rates [49]. This may be due in part to the beneficial effects of nuts on blood lipids [50] and other dis- Fig. 2. RAVLT scores across quintiles of urinary polyphenol excre- ease biomarkers, including oxidation, inflammation, and endothelial dysfunction [41]. Furthermore, higher intake of nuts has been related with better cognitive Olive oil is a major component of the traditional function and lesser cognitive decline in a prospective Mediterranean diet. It contains abundant monoun- study [51]. Our findings, together with those of a recent saturated fatty acids (MUFA), mostly oleic acid, experimental study showing that walnut supplementa- and, depending on the degree of refinement, variable tion improves both motor and cognitive function in C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging aged rats [52], point to the need for further studies on intake showed relationships in the expected direction [3, 5], except for those concerning cereal intake and There is consistent epidemiological evidence that physical activity. That cereal intake related inversely moderate consumption of alcohol relates inversely to to memory function might be due to the fact that risk of CHD and total mortality [53]. Among alco- little amounts of whole grains are consumed in holic beverages, wine possibly provides additional Spain. Refined grains have a high glycemic index cardiovascular benefits because it counteracts oxida- that is associated with insulin resistance, a covariate tive stress through its high polyphenolic content [54].
of cognitive dysfunction [5]. The inverse association In our study participants who consumed alcohol were between physical activity and verbal memory was mostly moderate wine drinkers, and the daily dose unexpected and is difficult to explain. Given the cross- of wine related to a better overall cognitive function sectional design of our study, it might be explained in them. These findings concur with the results of by reverse causation if participants at higher vas- other studies showing an association of moderate alco- cular risk, hence more prone to develop impaired hol consumption with better cognitive performance cognition, exercised more following advice of their and a reduced risk of neurodegenerative diseases [55, Our study has limitations. First, the sample size Because coffee, a beverage with high antioxidant is relatively small. Second, given the cross-sectional content, is commonly consumed in European Mediter- design of the study, we cannot exclude the possibility ranean countries, we assessed its association with of reverse causation or residual confounding. Third, the cognitive performance. The observed direct associ- neuropsychological test battery used does not include ation with verbal memory is consistent with prior all cognitive functions, although verbal memory, one evidence on the protective effect of caffeine against of the first areas to be affected with aging, was well assessed with RAVLT and WMS associated pairs.
A common characteristic of the foods directly Finally, our cohort was at a particularly high vascular related to cognitive performance in our study is their risk, thus the results may not be generalized to the aver- richness in polyphenols, highly bioactive molecules age elderly population. The study also has strengths, with beneficial effects that go beyond the modula- such as the wide between-subject variability of food tion of oxidative stress to improve brain function, at consumption, a comprehensive evaluation of cardio- least in experimental models of aging [58]. Indeed, vascular risk and dietary intake and, in particular, the urinary polyphenol excretion was independently asso- use of urinary polyphenols as an objective biomarker ciated with memory performance with a continuous, of intake that is not subject to the possibilities of bias dose-related effect. These findings, heretofore not described, support the validity of the observed asso- In conclusion, in the context of the Mediterranean ciations among antioxidant-rich foods and cognition.
diet, increasing consumption of antioxidant-rich Antioxidant-rich foods, but not total polyphenol excre- foods in general and of polyphenols in particular is tion, have been related to better cognitive performance associated with better cognitive performance in an also in other clinical studies [6, 26, 59–61]. Further- elderly cohort at high cardiovascular risk. The results more, animals fed antioxidant foods showed improved reinforce the notion that Mediterranean diet compo- cellular signaling and neuronal communication that nents might counteract age-related cognitive decline translated into better cognitive and motor perfor- [19, 21–23]. While causality cannot be inferred from results of a cross-sectional assessment such as the present one, antioxidant-rich foods are known for many beneficial properties with no harm, thus between urinary polyphenols and Uncorrected Author Proof they can be recommended to the general public to in our study is an additional argument in favor of promote better health, including probably better antioxidant-rich foods. Our results further support the cognitive function. The prospective examination general theory of oxidative stress as a major driv- of the whole cohort of the 6-year PREDIMED ing force for age-related neurodegenerative processes regarding the potential of the Mediterranean diet Other variables independently associated with cog- to counteract the effects of aging on cognitive decline nitive function in our study, such as gender, age, and reduce the incidence of neurodegenerative education years, diabetes, hypertension, and meat C. Valls-Pedret et al. / Polyphenol-Rich Foods and Cognition in Aging ACKNOWLEDGMENTS
Gu Y, Nieves JW, Stern Y, Luchsinger JA, Scarmeas N (2010) Food combination and Alzheimer disease risk. A protective diet. Arch Neurol 67, 699-706.
We thank the PREDIMED participants for their Serra-Majem L, Roman B, Estruch R (2006) Scientific willingness and enthusiasm to collaborate in the evidence of interventions using the Mediterranean diet: A study and Emili Corbella for providing expert assis- systematic review. Nutr Rev 64, S27-S47.
Mente A, de Koning L, Shannon HS, Anand SS (2009) A tance with statistical analyses. CIBERobn and RETIC systematic review of the evidence supporting a causal link RD06/0045 are initiatives of ISCIII, Spain. This between dietary factors and coronary heart disease. Arch study was supported by PI07-0954 from ISCIII Intern Med 169, 659-669.
and GVACOMP2010-181 from Generalitat Valen- Mart´ınez-Gonz´alez MA, Garc´ıa-L´opez M, Bes-Rastrollo M, Toledo E, Mart´ınez-Lapiscina EH, Delgado-Rodr´ıguez M, ciana (Prof Corella); AGL2010-22319-C03-01/02/03 V´azquez Z, Benito S, Beunza JJ (2011) Mediterranean diet (Drs Lamuela-Ravent´os and Medina-Rem´on); FIS and the incidence of cardiovascular disease: A Spanish cohort.
PI 07/0473 and AGL2007-66638-C02-01/02 (Dr Nutr Metab Cardiovasc Dis 21, 237-244.
Estruch); PI070240, PI070312, and PI081943 from Sofi F, Abbate R, Gensini GF, Casini A (2010) Accruing evi- dence about benefits of adherence to the Mediterranean diet ISCIII (Prof Mart´ınez-Gonz´alez).
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