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Title
Dietary polyphenol intake in Europe: the European Prospective Investigation into Cancer
and Nutrition (EPIC) study.
Permalink
https://escholarship.org/uc/item/5s8969wc
Journal
European journal of nutrition, 55(4)
ISSN
1436-6207
Authors
Zamora-Ros, Raul
Knaze, Viktoria
Rothwell, Joseph A
et al.
Publication Date
2016-06-01
DOI
10.1007/s00394-015-0950-x
Copyright Information
This work is made available under the terms of a Creative Commons Attribution License,
availalbe at https://creativecommons.org/licenses/by/4.0/
Peer reviewed
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ORIGINAL CONTRIBUTION
Dietary polyphenol intake in Europe: the European Prospective
Investigation into Cancer and Nutrition (EPIC) study
Raul Zamora-Ros
1
•
Viktoria Knaze
1
•
Joseph A. Rothwell
1
•
Bertrand He
´
mon
1
•
Aurelie Moskal
1
•
Kim Overvad
2
•
Anne Tjønneland
3
•
Cecilie Kyrø
1,3
•
Guy Fagherazzi
4,5,6
•
Marie-Christine Boutron-Ruault
4,5,6
•
Marina Touillaud
4,5,6
•
Verena Katzke
7
•
Tilman Ku
¨
hn
7
•
Heiner Boeing
8
•
Jana Fo
¨
rster
8
•
Antonia Trichopoulou
9,10
•
Elissavet Valanou
9
•
Eleni Peppa
9
•
Domenico Palli
11
•
Claudia Agnoli
12
•
Fulvio Ricceri
13
•
Rosario Tumino
14
•
Maria Santucci de Magistris
15
•
Petra H. M. Peeters
16,17
•
H. Bas Bueno-de-Mesquita
17,18,19,20
•
Dagrun Engeset
21
•
Guri Skeie
21
•
Anette Hjarta
˚
ker
22
•
Virginia Mene
´
ndez
23
•
Antonio Agudo
24
•
Esther Molina-Montes
25,26
•
Jose
´
Marı
´
a Huerta
26,27
•
Aurelio Barricarte
26,28
•
Pilar Amiano
26,29
•
Emily Sonestedt
30
•
Lena Maria Nilsson
31,32
•
Rikard Landberg
33,34
•
Timothy J. Key
35
•
Kay-Thee Khaw
36
•
Nicholas J. Wareham
37
•
Yunxia Lu
17
•
Nadia Slimani
1
•
Isabelle Romieu
1
•
Elio Riboli
17
•
Augustin Scalbert
1
Received: 11 February 2015 / Accepted: 2 June 2015 / Published online: 17 June 2015
Ó Springer-Verlag Berlin Heidelberg 2015
Abstract
Background/Objectives Polyphenols are plant secondary
metabolites with a large variability in their chemical
structure and dietary occurrence that have been associated
with some protective effects against several chronic dis-
eases. To date, limited data exist on intake of polyphenols
in populations. The current cross-sectional analysis aimed
at estimating dietary intakes of all currently known indi-
vidual polyphenols and total intake per class and subclass,
and to identify their main food sources in the European
Prospective Investigation into Cancer and Nutrition cohort.
Methods Dietary data at baseline were collected using a
standardized 24-h dietary recall software administered to
Electronic supplementary material The online version of this
article (doi:10.1007/s00394-015-0950-x) contains supplementary
material, which is available to authorized users.
& Augustin Scalbert
scalberta@iarc.fr
1
Biomarker Group, Nutrition and Metabolism Section,
International Agency for Research on Cancer (IARC), 150,
cours Albert Thomas, 69372 Lyon Cedex 08, France
2
Department of Public Health, Section for Epidemiology,
Aarhus University, Aarhus, Denmark
3
Danish Cancer Society Research Center, Copenhagen,
Denmark
4
U1018, Nutrition, Hormones and Women’s Health Team,
Inserm, Centre for Research in Epidemiology and Population
Health (CESP), Villejuif, France
5
UMRS 1018, Paris South University, Villejuif, France
6
Institut Gustave Roussy, 94805 Villejuif, France
7
Division of Cancer Epidemiology, German Cancer Research
Center, Heidelberg, Germany
8
Department of Epidemiology, German Institute of Human
Nutrition Potsdam-Rehbru
¨
cke, Nuthetal, Germany
9
Hellenic Health Foundation, Athens, Greece
10
Bureau of Epidemiologic Research, Academy of Athens,
Athens, Greece
11
Molecular and Nutritional Epidemiology Unit, Cancer
Research and Prevention Institute-ISPO, Florence, Italy
12
Nutritional Epidemiology Unit, Fondazione IRCCS Istituto
Nazionale dei Tumori, Milan, Italy
13
Center for Cancer Prevention (CPO-Piemonte), and Human
Genetic Foundation (HuGeF), Turin, Italy
14
Cancer Registry and Histopathology Unit, ‘‘Civic M.P.
Arezzo’’ Hospital, ASP Ragusa, Italy
15
Department of Clinical and Experimental Medicine, Federico
II University, Naples, Italy
16
Department of Epidemiology, Julius Center for Health
Sciences and Primary Care, University Medical Center
Utrecht, Utrecht, The Netherlands
17
School of Public Health, Imperial College London, London,
UK
123
Eur J Nutr (2016) 55:1359–1375
DOI 10.1007/s00394-015-0950-x
36,037 adult subjects. Dietary data were linked with Phe-
nol-Explorer, a database with data on 502 individual
polyphenols in 452 foods and data on polyphenol losses
due to cooking and food processing.
Results Mean total polyphenol intake was the highest in
Aarhus—Denmark (1786 mg/day in men and
1626 mg/day in women) and the lowest in Greece
(744 mg/day in men and 584 mg/day in women). When
dividing the subjects into three regions, the highest intake
of total polyphenols was observed in the UK health-
conscious group, followed by non-Mediterranean (non-
MED) and MED countries. The main polyphenol con-
tributors were phenolic acids (52.5–56.9 %), except in
men from MED countries and in the UK health-conscious
group where they were flavonoids (49.1–61.7 %). Coffee,
tea, and fruits were the most important food sources of
total polyphenols. A total of 437 different individual
polyphenols were consumed, including 94 consumed at a
level [1 mg/day. The most abundant ones were the caf-
feoylquinic acids and the proanthocyanidin oligomers and
polymers.
Conclusion This study describes the large number of
dietary individual polyphenols consumed and the high
variability of their intakes between European populations,
particularly between MED and non-MED countries.
Keywords Polyphenols Dietary intake Food sources
EPIC
Abbreviations
24-HDR 24-h dietary recall
EPIC European Prospective Investigation into
Cancer and Nutrition
MED Mediterranean
s.e. Standard error
SU.VI.MAX SUpple
´
mentation en VItamines et
Mine
´
raux AntioXydants
USDA US Department of Agriculture
Introduction
Polyphenols are plant secondary metabolites widely dis-
tributed in plant-based foods, such as tea, coffee, wine,
fruit, vegetables, whole-grain cereals, and cocoa [1].
Dietary polyphenols constitute a large family of [500
different compounds with highly diverse structures from
simple molecules, such as phenolic acids, to large ones,
such as proanthocyanidin polymers [1]. According to their
chemical structure, polyphenols are divided into four main
classes: flavonoids, phenolic acids, lignans, and stilbenes
[2]. In foods, flavonoids, lignans, and stilbenes are usually
found as glycosides, whereas phenolic acids are most often
present as esters with various polyols; some polyphenols
such as flavanols are mainly present as aglycones (free
18
Department for Determinants of Chronic Diseases (DCD),
National Institute for Public Health and the Environment
(RIVM), Bilthoven, The Netherlands
19
Department of Gastroenterology and Hepatology, University
Medical Centre, Utrecht, The Netherlands
20
Department of Social and Preventive Medicine, Faculty of
Medicine, University of Malaya, Kuala Lumpur, Malaysia
21
Department of Community Medicine, Faculty of Health
Sciences, UiT The Arctic University of Norway, Tromsø,
Norway
22
Department of Nutrition, Institute of Basic Medical Sciences,
University of Oslo, Oslo, Norway
23
Public Health Directorate, Asturias, Spain
24
Unit of Nutrition, Environment and Cancer, Cancer
Epidemiology Research Program, Catalan Institute of
Oncology, Barcelona, Spain
25
Escuela Andaluza de Salud Pu
´
blica, Instituto de
Investigacio
´
n Biosanitaria ibs, Granada, Hospitales
Universitarios de Granada/Universidad de Granada, Granada,
Spain
26
CIBER Epidemiologı
´
a y Salud Pu
´
blica (CIBERESP),
Madrid, Spain
27
Department of Epidemiology, Murcia Regional Health
Council, IMIB-Arrixaca, Murcia, Spain
28
Navarre Public Health Institute, Pamplona, Spain
29
Public Health Department of Gipuzkoa, BioDonostia
Research Institute, Health Department of Basque Region,
San Sebastia
´
n, Spain
30
Department of Clinical Sciences, Lund University, Malmo
¨
,
Sweden
31
Department of Nutritional Research, Public Health and
Clinical Medicine, Umea
˚
University, Umea
˚
, Sweden
32
Arcum, Arctic Research Centre at Umea
˚
University, Umea
˚
,
Sweden
33
Department of Food Science, Uppsala BioCentre, Swedish
University of Agricultural Sciences, Uppsala, Sweden
34
Nutritional Epidemiology Unit, Institute of Environmental
Medicine, Karolinska Institutet, Stockholm, Sweden
35
Cancer Epidemiology Unit, University of Oxford, Oxford,
UK
36
Department of Public Health and Primary Care, University of
Cambridge, Cambridge, UK
37
MRC Epidemiology Unit, Institute of Metabolic Science,
Cambridge University, Cambridge, UK
1360 Eur J Nutr (2016) 55:1359–1375
123
forms) [1]. It is important to consider these structural
variations as glycosylation/esterification greatly influences
polyphenol absorption in the gut and bioavailability [3].
Over the last two decades, the literature on polyphenols has
grown exponentially following the recognition of their
antioxidant, anti-inflammatory, and anti-carcinogenic
properties and more evidence for their potential beneficial
effects upon health has been accumulated [4]. However,
epidemiological data on the relationship between
polyphenol intake and the risk of chronic diseases and
mortality are still limited, especially in prospective studies,
and largely concern flavonoids and lignans [2, 5–7]. To
calculate polyphenol intake, most of these studies have
used the US Department of Agriculture (USDA) databases
on polyphenol contents in foods [8–10], which only contain
data on flavonoids expressed as aglycones. The more
recently published Phenol-Explorer database (www.phe
nol-explorer.eu)[11] is more comprehensive and gathers
food composition data on all known polyphenols, either
aglycones, glycosides or esters depending on how they are
found in foods. Moreover, a new module of the Phenol-
Explorer database contains data on the effects of cooking
and food processing on polyphenol contents [12]. These
retention factors permit to take into account the effects of
food cooking and processing measurements when calcu-
lating polyphenol intake and to improve the reliability of
such measurements [13].
Several descriptive papers on intakes of flavonoids and
other polyphenols have been published using either the
USDA databases [14–16], the Phenol-Explorer database
[17–19] or custom databases [20]. The purpose of the present
work is to describe intake of all currently known dietary
polyphenols in several European countries using the more
comprehensive Phenol-Explorer database and especially
applying polyphenol-specific retention factors. The Euro-
pean Prospective Investigation into Cancer and Nutrition
(EPIC) study offers a unique opportunity to estimate the
intake of individual polyphenols, to identify their main food
sources, and to compare these intakes between different
European countries showing large variations in diets.
Materials and methods
Study population
The EPIC study is a large cohort study conducted in 10
European countries (Denmark, France, Germany, Greece,
Italy, Norway, Spain, Sweden, the Netherlands, and the
UK) and aims at investigating the role of diet and envi-
ronmental factors on the etiology of cancer and other
chronic diseases [21, 22]. Over half million participants
were recruited mostly from the general population residing
within defined geographical areas, with some exceptions:
women of a health insurance company for teachers and
school workers (France), women attending breast cancer
screening (Utrecht—the Netherlands and Florence—Italy),
mainly blood donors (most centers in Italy and Spain) and a
cohort consisting predominantly of vegetarians (the
‘‘health-conscious’’ group in Oxford, UK) [22]. The initial
23 EPIC administrative centers were redefined into 27
geographical regions relevant to the analysis of dietary
consumption patterns [23].
Data used in the present work were derived from the EPIC
calibration study, in which a 24-h dietary recall (24-HDR)
was administered. The cohort comprises an 8 %
(n = 36,994) random sample stratified by age, sex, and
center, and weighted for expected cancer cases in each
stratum of the whole EPIC cohort [23]. After exclusion of
941 subjects who were aged younger than 35 years or older
than 74 years because of low participation in these age cat-
egories, and 16 individuals due to incomplete dietary infor-
mation, 36,037 participants were included in the present
analysis. Approval for the study was obtained from ethical
review boards of the International Agency for Research on
Cancer (IARC) and from all local participating institutions.
All participants provided written informed consent.
Dietary and lifestyle information
Dietary assessment was performed with a single 24-HDR
using specialized software (EPIC-Soft) [24], and adminis-
tered in a face-to-face interview, except in Norway, where it
was obtained by telephone interview [25]. Data on age, as
well as on body weight and height, were self-reported by the
participants during the 24-HDR interview. Data on other
lifestyle factors, including educational level, physical
activity, and smoking history, were collected at baseline
through standardized questionnaires [23, 26]. The mean
time interval between completion of the baseline ques-
tionnaire measures and the 24-HDR interview varied by
country, and ranged from the same day to 3 years later [23].
Food composition database on polyphenols
The Phenol-Explorer database provides data on 502
polyphenol compounds in 452 plant-based foods collected
from 638 scientific peer-reviewed articles [11]. All animal
foods that contain none or only traces of plant polyphenols
were excluded.
Phenol-Explorer contains data on four main polyphenol
classes: flavonoids, phenolic acids, stilbenes, and lignans, as
well as on a number of miscellaneous minor polyphenols that
include tyrosols, alkylphenols (mainly alkylresorcinols), and
alkylmethoxyphenols among others, described in the Phe-
nol-Explorer database and in this manuscript as ‘‘other
Eur J Nutr (2016) 55:1359–1375 1361
123
polyphenols’’ [11]. Total polyphenol content was calculated
as the sum of the contents of individual compounds expres-
sed in mg/100 g food fresh weight. The data used in the
present study were mainly acquired by chromatography
without previous hydrolysis of the food extracts except for a
few polyphenols bound to the food matrix. Lignans in all
foods, ellagic acid in walnuts, and hydroxycinnamic acids in
cereals, legumes, and olives were quantified by chromatog-
raphy after previous basic or acid hydrolysis. Proantho-
cyanidin dimers were measured as individual compounds by
chromatography without prior hydrolysis, whereas other
proanthocyanidin oligomers (trimers, 4–6 and 7–10 oligo-
mers) and proanthocyanidin polymers were measured as
mixtures by normal-phase HPLC. Overall data on 463 indi-
vidual polyphenols were used.
Some missing polyphenol content values for orange fruit
and breakfast cereals were extrapolated from orange juice
and wheat flour, respectively. The polyphenol content of
different types of coffee, ‘‘American’’ or filtered diluted
coffee and espresso, reported in the 24-HDR, was esti-
mated by multiplying the polyphenol contents of ‘‘normal’’
filtered coffee from the Phenol-Explorer database by 0.4
and 2, respectively [27, 28]. When the type of herbal tea
was unspecified in the 24-HDRs, the polyphenolic com-
position of a mix of herbal tea was applied on a country-by-
country basis. The effect of food cooking and processing
was accounted for by applying polyphenol-specific reten-
tion factors from Phenol-Explorer [12] to 24-HDR foods
wherever relevant. Phenol-Explorer contains data on 1253
aggregated retention factors, including data on 161
polyphenols and 35 processes, such as domestic cooking,
storage, and industrial processing.
Statistical analyses
Dietary polyphenol intakes were estimated using general
linear models and presented as means and standard errors
(s.e.) stratified by sex and center, adjusted for age, and
weighted by season and weekday of the 24-HDR to control
for different distributions of participants across seasons and
24-HDR days. The contribution of each polyphenol class,
subclass, and family to the total polyphenol intake was
calculated as a percentage according to three ad hoc
European regions: (1) Mediterranean (MED) countries: all
centers in Greece, Spain, Italy, and the south of France; (2)
non-MED countries: all centers in the north-east and north-
west of France, Germany, the Netherlands, UK general
population, Denmark, Sweden, and Norway; (3) UK
health-conscious group. The contribution of each food
group to the intake of total and polyphenol classes by
European region was also calculated as a percentage.
Differences in polyphenol intakes stratified by European
region were also compared using general linear models
according to the categories of sex, age (35–44, 45–54,
55–64, and 64–74), BMI (\25, 25–30, and [30 kg/m
2
),
educational level (no formal education, primary school,
technical/professional school, secondary school, university,
or not specified), smoking status (never, former, current
smoker, and not specified), and Cambridge physical
activity index (inactive, moderately inactive, moderately
active, and not specified). All these models were adjusted
for sex, age (years), center, BMI (kg/m
2
), and energy
intake, and weighted by season and day of 24-HDR.
P values \0.05 (two-tailed) were considered significant.
All analyses were conducted using the SPSS Statistics
software (version 19.0; SPSS Inc.).
Results
A south-to-north gradient in the daily mean intake of total
polyphenols was observed among EPIC centers, in both men
and women (Fig. 1). The highest total polyphenol intake in
both sexes was in Aarhus—Denmark (in men 1786 mg/day
and in women 1626 mg/day), whereas the lowest intake was
in Greece in both men (744 mg/day) and women
(584 mg/day). Table 1 shows the mean intakes of total
polyphenols and polyphenol classes adjusted for sex, age,
BMI (except where stratified for these variables), center, and
energy intake, and weighted by season and weekday of the
24-HDR. The intake of phenolic acids, stilbenes, and other
polyphenols was higher in men than in women, whereas for
flavonoids and lignans the opposite was observed. No differ-
ences were observed for total polyphenol intake between men
and women. The intake of flavonoids, stilbenes, lignans, and
other polyphenols increased with age, whereas the opposite
was seen for total polyphenols and phenolic acids for which a
maximum intake was observed at the age of 45–54 years.
When comparing the intake by European region, the UK
health-conscious group (1521 mg/day) had the highest intake
of total polyphenols due to the higher intake of flavonoids.
Non-MED countries (1284 mg/day) showed a higher total
polyphenol intake when compared to MED countries
(1011 mg/day), with phenolic acids as the main contributors.
MED countries presented the highest intake of stilbenes
compared to the other regions. Individuals with BMI \ 25,
and/or a university degree, and/or current smokers showed the
highest intakes of total polyphenols. No differences in total
polyphenol intake were observed between groups showing
different physical activity levels (Table 1).
Phenolic acids were the main contributors to the total
polyphenol intake in non-MED countries (57 and 53 % in
men and women, respectively) and in women from MED
countries (54 %) (Table 2). Flavonoids were the second
most abundant contributors in these groups (38–44 %). In
contrast, in the UK health-conscious group and in men
1362 Eur J Nutr (2016) 55:1359–1375
123
