Adherence to the Mediterranean Diet in children and adolescents: A systematic review

Accepted Manuscript Adherence to the Mediterranean Diet in Children and Adolescents: A Systematic Review P. Iaccarino Idelson, L. Scalfi, G. Valerio PII:

S0939-4753(17)30003-0

DOI:

10.1016/j.numecd.2017.01.002

Reference:

NUMECD 1691

To appear in:

Nutrition, Metabolism and Cardiovascular Diseases

Received Date: 21 July 2016 Revised Date:

31 December 2016

Accepted Date: 3 January 2017

Please cite this article as: Iaccarino Idelson P, Scalfi L, Valerio G, Adherence to the Mediterranean Diet in Children and Adolescents: A Systematic Review, Nutrition, Metabolism and Cardiovascular Diseases (2017), doi: 10.1016/j.numecd.2017.01.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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ADHERENCE TO THE MEDITERRANEAN DIET IN CHILDREN AND ADOLESCENTS: A SYSTEMATIC REVIEW Iaccarino Idelson P1, Scalfi L1, Valerio G2 1

ples, Italy

Corresponding author Paola Iaccarino Idelson

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Department of Public Health, School of Medicine Federico II University of Naples, Naples, Italy [email protected] mobile ++39.3494271286 fax: not available Postal address Via Sergio Pansini 5, 80131 Napoli (Italia)

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Department of Public Health, School of Medicine, Federico II University of Naples, Naples, Italy. 2 Department of Movement Sciences and Wellbeing. Parthenope University of Naples, Na-

Structure summary 247 words

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5764 words

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Abstract

Keywords

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102 references, 5 Tables and 1 Figure

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Mediterranean Diet; Adherence; Children; Adolescents; Indexes; Score.

Acronyms

BIA=bioelectrical impedance analysis; BMI=body mass index; FFQ=food frequency questionnaire; fMDS= food frequency-based Mediterranean Diet Score; IOTF=International Obesity Task Force; IPAQ=International Physical Activity Questionnaire; MD=Mediterranean Diet; MDS=Mediterranean Diet Score, MUFA=monounsaturated fatty acids; PA=physical activity, SES=socioeconomic status; SFA=saturated fatty acids; STROBE=strenghtening the reporting of observational studies in epidemiology statement; WC=waist circumference; WHO=World Health Organization.

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ABSTRACT Background and Aim A decreased adherence to the Mediterranean Diet (MD) may be related to a rise in chronic non-communicable diseases from childhood onward. The aim of this systematic review was to summarize the available literature regarding MD adherence in children and adolescents,

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and focusing, more specifically, on the association of MD adherence with demographic and anthropometric variables, body composition, lifestyle, and diet adequacy.

Methods and results

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A search of scientific literature was carried out on PUBMED, SCOPUS, Clinical Trials Results, Google Scholar, and British Library Inside for studies published in the last 20 years.

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Fifty-eight papers were finally included according to the following criteria: MD adherence evaluated through a quantifying score or index, age 2-20 years, sample size >200 participants, observational or intervention studies regarding the general population. The KIDMED index was the most widely used scoring system. MD adherence widely varied within the Mediterranean countries for both children and adolescents, with also large differences among various European countries, while few data are available for non-Mediterranean

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countries. Most of the eligible studies showed that MD adherence was directly associated with physical activity (and possibly with diet adequacy) and inversely with sedentary behav-

sistent. Conclusions

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ior, while the results for gender, age, socioeconomic status and weight status were not con-

Further validation of MD indexes in terms of reproducibility and consistency with the MD is

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needed. At the same time, more prospective cohort and intervention studies may better elucidate the relationships of MD adherence with behavioral and health outcomes.

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INTRODUCTION The term “Mediterranean Diet” (MD) has been widely used to describe the traditional dietary habits of people living around the Mediterranean Sea, in particular in the olive tree growing areas. MD is defined by the prevalent consumption of fruit, vegetables, whole grain cereals,

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legumes, nuts and seeds, with olive oil as the main source of added fat. Other characteristics of MD are regular but moderate intake of dairy products (milk, yoghurt and cheese), low to moderate intake of fish and poultry meat, little red meat, and moderate wine drinking (at meals)1,2. The use of local and traditional food products, seasonality, and biodiversity are other features of interest, while representative cultural and lifestyle elements are frugality,

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sobriety, conviviality, typical recipes, and moderate to high physical activity (PA)3. With respect to nutrients, the MD is first of all characterized by high intake of low glycaemic index

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carbohydrates, monounsaturated fatty acids, dietary fiber and antioxidants, and by both the consumption of vegetable proteins and a balanced ratio of n-6:n-3 fatty acids. It is generally thought that the declining adherence to the MD (MD adherence) in the Mediterranean Countries over the last decades, in parallel with a shift towards a Western dietary pattern, may be associated with the incidence of chronic non-communicable diseases from childhood onward4. The most outstanding event has been the rise of pediatric obesity, which

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often tracks into adulthood, increasing the risk of developing cardiovascular disease, type 2 diabetes and other chronic diseases5. Excess body fat has been attributed to both high intake of energy-dense, nutrient-poor foods and beverages, such as chips, salted snacks, candies,

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and soft drinks, and a sedentary behavior 6,7. On the other hand, regular PA and a diet high in fruit, vegetables, legumes and whole-grain cereals have been shown to be protective against weight gain 7,8. MD, on the whole, has been proposed, and is commonly accepted, as a likely

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dietary model for the prevention and control of chronic non-communicable diseases over the entire lifespan 9,10.

In assessing the relationships between health and diet, a particular interest has emerged to develop tools that approximate the overall adherence to certain dietary patterns. For example, the evaluation of MD adherence is made possible by using specific indexes (or scoring systems), and this is true not only in adults 11, but also in the first two decades of life. On the basis of scientific evidence, MD adherence indexes aim to capture the essence of MD taking into consideration the intake of specific foods/nutrients or food habits to derive scores which may be used to categorize subjects and have been shown to be significantly related with health outcomes. 3

ACCEPTED MANUSCRIPT While the use of MD adherence indexes in adults has been reviewed11, no systematic data on this issue have so far been produced for the first two decades of life. The aim of this systematic review was to summarize the available literature focusing on MD adherence, as assessed using specific indexes, in children and adolescents, and, more specifically, on the association of MD adherence with demographic and anthropometric variables,

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body composition, lifestyle, food groups, and diet adequacy.

METHODS LITERATURE SEARCH

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The protocol of our systematic review followed PRISMA and Cochrane Guidelines, as much as possible for our study design 12,13.

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We focused the search on studies referring to MD adherence, evaluated with an index in the first two decades of life and published between 1st January 1996 and 31st December 2015. In order to perform a comprehensive search of the literature, two independent researchers (PII and GV) explored PUBMED and SCOPUS for peer reviewed papers, and Clinical Trials Results, Google Scholar, British Library Inside for the grey literature. Search terms in PUBMED were identified by exploring the following major and MeSH subjects terms: "MEDI-

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TERRANEAN DIET"[All Fields] AND (("child"[MeSH Terms] OR "child"[All Fields] OR "children"[All Fields]) OR ("adolescent"[MeSH Terms] OR "adolescent"[All Fields] OR "adolescents"[All Fields])) AND (ADHERENCE[All Fields] OR SCORE[All Fields] OR ("abstracting and indexing as topic"[MeSH Terms] OR ("abstracting"[All Fields] AND "in-

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dexing"[All Fields] AND "topic"[All Fields]) OR "abstracting and indexing as topic"[All Fields] OR "index"[All Fields])). Search terms in the other databases were the following:

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“Mediterranean diet”, “children”, “adolescents”, “index”, “score”, and “adherence”. To identify as many studies as possible our search strategy was not restricted to English-language publication only. Moreover, references of eligible articles and systematic reviews were examined for additional relevant studies while reviews, editorials and comments were considered only for discussion.

DATA EXTRACTION AND QUALITY ASSESSMENT After records’ identification through database searching and other sources, the systematic selection process was performed in 3 phases, to minimize bias and to ensure that all relevant 4

ACCEPTED MANUSCRIPT studies were included (see the flow diagram in Figure 1). The inclusion criteria were the following: adherence to the MD through a quantifying score or index, age of participants between 2 and 20 years, sample size > 200 participants, observational or intervention studies regarding the general population. Articles were screened by evaluating titles and abstracts, thereafter the selected papers were read in full for final eligibility by all the authors, who also

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solved discrepancies by discussion. The following data were recorded for each selected article and tabulated in an excel file: authors and year of publication, study settings and design, subjects’ characteristics such as age and gender, sample size, methodology used to assess MD adherence, primary and secondary

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endpoints. These data were recorded by PII and cross-checked by the other 2 authors to identify any error. The quality of included studies (including potential sources of bias) was assessed individually by PII and GV, and then reviewed by the other author (LS) using the

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Strengthening the Reporting of Observational Studies in Epidemiology Statement (STROBE) checklist, whose final score varied from 0 to 3414. Again, any discrepancy was discussed until a decision was reached with 100% agreement.

LITERATURE-BASED INDEXES TO ASSESS MD ADHERENCE IN CHILDREN AND ADOLES-

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MD adherence indexes evaluate different items, i.e. the intake of various nutrients/foods and specific food habits, for example having breakfast or fast food consumption, to derive a score which may be used to categorize subjects. The components of an index were selected on the

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basis of scientific evidence and a priori recognized characteristics of MD. Indexes vary for number of components, question content, scoring system, contribution (positive or negative)

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of a single component to the total score, and category classification system11. To the best of our knowledge, the MD adherence indexes applied in children and adolescents have been the following: a) KIDMED score15; b) adapted versions of the Mediterranean Diet Score (MDS) derived from the original tool, which was proposed by Thricopoulou et al.16-20; and c) food frequency-based Mediterranean Diet Score (fMDS)21. The KIDMED index was developed by Serra-Majem et al.15 in subjects aged 2–24 years, focusing on specific food habits of the Mediterranean tradition. The questionnaire can be selfadministered or filled in by interview, or information may be obtained using a more general tool to assess dietary habits (for example, a food frequency questionnaire, FFQ). The KIDMED score is calculated from 16 yes/no questions. Most of them concern the consumption of different food groups: a fruit/fruit juice every day (question 1); a second fruit 5

ACCEPTED MANUSCRIPT every day (question 2); vegetables regularly once a day (question 3); vegetables more than once a day (question 4); fish at least 2–3 times per week (question 5); legumes more than once a week (question 7); pasta/rice 5 or more times per week (question 8); nuts at least 2–3 times per week (question 10); regular use of olive oil at home (question 11); two yoghurts/some cheese daily (question 15); sweets and candy several times every day (question

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16). There are also four questions on breakfast: cereals or grains for breakfast (question 9); skipping breakfast (question 12); a dairy product for breakfast (question 13); commercially baked goods or pastries for breakfast (question 14). Finally, question 6 asks about going to a fast-food restaurant more than once a week.

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For each “yes” response one point is given to answers representing positive food habits (items 1-5, 7-11, 13, 15), and one point is subtracted for those representing negative food habits (items 6, 12, 14, 16). Three categories of adherence (good, average and poor) were de-

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fined15 according to a score ≥8, between 4 and 7, and ≤3.

In 3 papers22-24 slightly modified versions of KIDMED were used. In particular, since that information was not available, Chatzi et al.22 omitted the items about the consumption of fast foods, sweets and legumes, considering the intake of red meat as an additional negative component, while Monjardino et al.23 excluded the items regarding breakfast. On the other hand,

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Roccaldo et al.24 eliminated the item regarding going to fast food restaurants, because these latter were not uniformly distributed in the Italian areas investigated. The MDS index, which was based on some typical characteristics of the traditional Greek MD, was originally proposed for adults in 1995 by Trichopoulou et al.16 and later revised by

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the same authors adding fish consumption as a further protective component18. Information on the intake of foods and nutrients has commonly been obtained using a FFQ. There were

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seven protective components: high intake of grains (including bread and potatoes); vegetables; fruit; legumes; adequate intake of fish; moderate assumption of alcohol; high ratio of monounsaturated to saturated fats (MUFA:SFA). The two detrimental components were defined as high intakes of meat/meat products or milk/dairy products. Median value for each component, as calculated in the group of subjects participating in the study, was used as cutoff point16 (with the exception of alcohol, for which conventional cut-offs were used); for each item 1 point was given if the subject’s value was above or below the cut-off point for protective components and detrimental components, respectively. Thus, the original MDS score may vary from 0 (minimal adherence) to 9 (maximum adherence). The MDS index has been used in a number of studies on children/adolescents, but, apparently, only in one paper in its original version25. In some studies the component alcohol was re6

ACCEPTED MANUSCRIPT moved or considered to be detrimental26-35, or the components MUFA/SFA and/or milk/dairy products were eliminated26-29,35. In other cases some additional components were included (for example, the consumption of fast/junk foods or poultry26-29,33). Moreover, Jennings et al.30 considered dairy products as protective, while Tognon et al.20,21 classified legumes in the vegetables and evaluated the ratio between unsaturated fats (instead of MUFA) and SFA.

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The scoring system of MDS was also modified by several authors. Garcia-Marcos et al.28 generated a scoring system based on the frequency of intake: protective foods were rated 0 points = never or occasionally; 1 point=1-2 times/week; 2 points≥3 times/week, while nonprotective foods were rated 0 points≥3 times/week; 1 point=1-2 times/week; 2 points=never

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or occasionally. Other authors31,32,34,36,37 calculated a MDS score by computing a weighed Zscore from the distribution of values for each index component as observed in the subjects participating in the study. Z-scores for protective dietary components were added and those

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for detrimental dietary components were subtracted. The weighed Z-score so obtained was converted to relative percentage of adherence (0-100) using as reference the distribution of weighed Z-score values among the subjects studied17.

Finally, the fMDS has been used by Tognon et al.21. The relative frequencies of six food groups (with respect to the consumption of all food items) were categorized according to sex-

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specific and age-specific medians (calculated on the whole cohort). One point was given for intakes higher than median frequencies with respect to vegetables/legumes, fruit/nuts, cereals and fish, and for intakes below the median for dairy products and meat products. The final

>3.

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RESULTS

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score added up to a maximum of 6 points. High adherence levels were defined by a fMDS

DESCRIPTION OF PAPERS

The selection procedure is summarized in Figure 1. The first search on titles and abstracts led to 270 articles; 173 articles were excluded because they did not overtly meet the inclusion criteria. Out of the remaining 97 articles read in full, 39 papers were excluded because of subjects’age (n=5), low sample size (n=7), no adherence data (n=13), not focusing on MD (n=2), groups with special characteristics (n=2), reviews/commentaries/letters (n=10). We finally analyzed 58 papers15,20-76, which are summarized in Table 1 (55 cross-sectional studies, 2 cross-sectional plus prospective studies, and 1 cross-sectional plus intervention study), 8 of which in Spanish31,37,42,43,50,60,65,67, all including both male and female individuals. 7

ACCEPTED MANUSCRIPT As shown in Table 1, 43 studies used the KIDMED score, which was determined using the questionnaire in 27 studies or indirectly from a FFQ in 16 studies. In other 14 studies the different MDS versions, as above described, were applied (Table 1), and in 1 study the fMDS. As a whole, the studies involved 137,846 subjects with a sample size varying from 20074 to 20,106 individuals28. According to the STROBE checklist, the median quality score was 15

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(25th percentile=11.5 and 75th percentile=16.5). No articles were published until 2003, a single paper was published in 2003, another one in 2004, 2 in 2007, 3 in 2008, 6 in 2009, 7 in 2010, 11 in 2011, 3 in 2012, 8 in 2013, 12 in 2014, and finally 4 articles in 2015 (Table 1).

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The vast majority of papers presented data from the Mediterranean countries (19 from Greece, 22 from Spain, 4 from Italy, 4 from Cyprus, and 1 from Turkey). Moreover, there were 5 papers on other countries (3 in Portugal, 2 in the United Kingdom, 1 in Mexico) and 2

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multi-centre studies performed in the same cohorts from 8 European countries20,21 (Table 1). Ten papers and 35 papers provided data either on the first (children) or the second decade of life (adolescents) respectively, 13 papers showed data on both children and adolescents, 5 of which separately on the two groups and 8 on pooled data (Table 1). Excluding the studies with pooled data, the total number of subjects participating in the studies was 52,977 for chil-

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dren and 55,478 for adolescents.

MD ADHERENCE

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Results on MD adherence (as mean and/or median and/or distribution of categories) which were available from the selected papers are shown in Table 2: in 42 studies, out of 53, data

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were shown for the whole population, while in 11 studies they were reported only by gender (4 studies), rural/urban setting (4 studies), weight status (2 studies), or consumption of functional foods (1 study).

The KIDMED score was used in 38 studies (Table 2). Sixteen studies expressed the results as mean values, which varied from 3.6 in Greek adolescents49 to 7.60 in Spanish children67. In 30 studies (Table 2) the distribution of KIDMED categories (poor, average and good) was reported. With respect to the whole population, poor adherence varied from 1.6% in Spanish children63 to 62.8% in Greek adolescents62, average adherence from 28.0% in Greek adolescents74 to 73.8% in rural Italian adolescents53 and good adherence from 4.3% in Greek 10-12 year old subjects49 to 53.9% in Spanish children67. 8

ACCEPTED MANUSCRIPT Different MDS versions were used in 14 studies (Table 2). Four studies25,27,30,33 used a scoring system ranging from 0 to 8 or 9, while in 3 other studies26,28,29 the scoring range was 022. Five studies reported a mean MD adherence between 46.7% to 62.7%31,32,34,36,37 (scoring range 0-100), considering the weighed Z-values for detrimental and protective nutrients/foods. Other studies subdivided the population into categories: Santos et al.35 reported

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low adherence in 51.3% of subjects (two categories), while Noale et al.33 reported low adherence in 38.6%, moderate adherence in 47.4% and high adherence in the remaining 14.0% of subjects.

Finally, Tognon et al. in a multi-center study involving 8 European countries found different results depending on the adherence index used: for example, the proportion of children with

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high MD adherence ranged from 24.2% in Cyprus to 56.7% in Sweden using fMDS21, and

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from 29.4% in Germany to 49.3% in Italy using an adapted MDS20.

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ACCEPTED MANUSCRIPT FACTORS ASSOCIATED WITH MD ADHERENCE Gender Thirthy-three studies15,20,23-25,30-34,36,37,39,42,44,49-51,53,54,56,58,60,62-69,74,76 analyzed the between gender differences in MD adherence and gender (in 3 papers as predetermined primary endpoint32,50,66). Only 7 studies found a significant difference between genders: 6 studies report-

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ed a higher adherence in girls20,32,44,54,63,74, while the opposite was reported by Grao-Cruces et al.51

Age Twenty-four studies15,20,21,29,31-34,36,39,42-44,49,50,54,58,60,63-66,70,74 provided data on the association

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between MD adherence and age (in 4 cases as predetermined primary endpoint32,50,54,66). Eleven studies found a detrimental trend in MD adherence with age21,29,32,42-44,50,54,60,65,66

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which was significant in nine studies21,42-44,50,54,60,65,66. Socio-economic status

Twenty studies15,20,23,24,32,34,35,38,39,44,46,53,54,58,66,68-70,73,74 analyzed the association between MD adherence and SES (in 4 studies as predetermined primary endpoint38,46,66,73), mostly through the assessment of parents’ education, occupation, or both. Fifteen studies found a significant positive correlation between MD adherence and SES15,23,24,35,38,39,44,46,53,54,66,68-70,73. In particu-

mother’s education level. Urbanization

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lar, 7 studies15,24,44,66,68-70 found that a higher MD adherence was associated with a better

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Only 6 studies42,50,52,53,57,58 evaluated MD adherence in urban/rural settings, with 3 stud-

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ies50,52,53 reporting a significantly higher MD adherence in rural areas.

ASSOCIATION BETWEEN MD ADHERENCE AND ANTHROPOMETRIC VARIABLES OR BODY COMPOSITION

As summarized in Table 3, 26 papers provided data on the association between MD adherence and anthropometric variables or body composition. KIDMED index was used in 20 studies, MDS in 5 and fMDS in the other one. Four papers54,55,58,59 were carried out in the same group of individuals, each evaluating different endpoints. All studies were crosssectional with the exception of those by McCourt et al.25 and Monjardino et al.23 (crosssectional and prospective), and that by Tognon et al.21 (cross-sectional and intervention). In 10

ACCEPTED MANUSCRIPT this latter (European multi-center survey), the assessment of MD adherence was performed at baseline and was repeated two years after a community-based intervention focused on diet, physical activity and stress-coping capacity was implemented in selected regions from each country. Height and weight were directly measured in 17 studies and reported (by children, adoles-

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cents, or by their parents) in the other studies. Body Mass Index (BMI) was taken into account as endpoint in all studies, while 8 studies measured waist circumference (WC) and 6 studies fat mass (4 by bioimpedance analysis-BIA, and 2 by skinfold thickness). In 20 papers subjects were ranked according to weight categories (17 according to International Obesity Task Force criteria-IOTF77, 2 according to World Health Organization (WHO)78, and 1 ac-

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cording to Italian reference values79).

Eleven studies reported a significant association between MD adherence and BMI or obesity

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status, which was negative in 10 studies21,28,53,55,58,59,61,65,67,70 and positive in the other one64. In two studies, MD adherence was associated with obesity only in girls but not in boys58, or in adolescents but not in children55.

On the other hand, only 2 studies reported data on the significant association between MD adherence and underweight34,69. Ozen et al.34 showed that underweight adolescents who consumed functional foods had a higher risk of low MD adherence, while the opposite was ob-

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served among those who did not consume functional foods. Santomauro et al.69 found that poor MD adherence was more frequent in underweight subjects compared to overweight or obese adolescents.

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Three out of 8 studies found a significant association between MD adherence and WC, which was negative in 2 studies61,70 and positive in the other one64. Regarding the association be-

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tween MD adherence and body fatness, only 1 out of 6 studies21 found a negative association between fMDS and percentage of body fat estimated by triceps and subscapular skinfold thickness.

With reference to the two prospective studies, Monjardino et al.23 found no meaningful association between tertiles of adherence to the MD pattern and mean BMI in adolescents after 4 years of follow-up; similarly, McCourt et al.25 found no longitudinal relationship between the change in MD adherence and the change in BMI in 12–15-year olds and in the same individuals at 20–25 years of age. Finally, in the intervention study by Tognon et al.21 high MD adherence at baseline protected against the increase in BMI or WC, and more weakly in fat mass, independently of the intervention. 11

ACCEPTED MANUSCRIPT ASSOCIATION BETWEEN MD ADHERENCE AND LIFESTYLE VARIABLES As summarized in Table 4, 21 studies analyzed the association between MD adherence and lifestyle variables in terms of PA and/or sedentary behavior. In 7 studies32,48,50,54,60,66,69 this was considered as a predetermined primary endpoint. PA level was assessed through a questionnaire in 17 studies, while Jennings et al.30 used ac-

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celerometry as an objective tool. Fourteen studies reported a significant positive association between MD adherence and PA levels23,25,30,32,39,49,50,53,60,62,64,66,69,70. In addition, Arriscado et al.39 found a significant increase in aerobic capacity in the subjects with high MD adherence using the 20-m Shuttle Run test.

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Sedentary behavior was assessed in 11 studies evaluating the time allocated to television and/or personal computer and/or videogames24,32,33,39,48,50,54,58,64,66,69. Ten studies focusing on that issue showed a significant association between better MD adherence and less time spent

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in sedentary behavior24,32,39,48,50,54,58,64,66,69.

ASSOCIATION BETWEEN MD ADHERENCE AND FOOD GROUPS, NUTRIENTS AND ENERGY INTAKE

Thirteen studies evaluated and found a significant association between MD adherence and both32,53,70.

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diet adequacy (Table 5) in terms of food groups34,40,58, nutrients/energy23,30,33,54,62,71,72, or A positive association with MD adherence was found for the intake of energy23,30, carbohydrates33,53, protein70, dietary fiber33,53,54,70,72, vitamins33,54,72 and minerals23,33,54,62,72. In addi-

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tion, the 3 studies analyzing the intake of different fatty acids32,33,53 found a negative relationship with SFA intake and a positive association with MUFA:SFA ratio. Moreover, Schröder

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et al.71 reported a negative association between MD adherence and higher energy density diSix studies analyzed the association between MD adherence and food groups32,34,40,53,58,70. A positive association was found with “pro-Mediterranean” foods, such as fruit, vegetables, fish, legumes, cereals etc.32,53,58,70, while negative relationships emerged with “antiMediterranean” foods, such as meat, salty snacks, sweets etc.32,40,53,70. Specifically, Ozen et al.34 reported a positive association between MD adherence and functional food intake.

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DISCUSSION Guidelines and recommendations from scientific experts and institutions strongly support the concept that a Mediterranean-like dietary pattern may reduce the risk of chronic noncommunicable diseases since childhood80-82. Thus, evaluating MD adherence and its deter-

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minants is crucial to design strategies for the implementation of a healthy diet in the general population and more specifically in the first two decades of life. This systematic review has examined the literature regarding MD adherence in children and adolescents, as assessed by using specific indexes and, more specifically, focusing on its association with demographic and anthropometric variables, body composition, lifestyle, food groups, and diet adequacy.

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MD adherence indexes for children and adolescents, either specifically developed or modified from those used in adults11,16, are designed to capture the essence of the MD pattern11.

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They were created according to a priori subjective criteria, indeed supported by scientific knowledge and evidence, and differ from each other in terms of number of items, question content, cut-off values, and so on. MD adherence is always evaluated through a score, by assessing both the frequency of consumption of different foods (sometime local food such as pasta or nuts) and other characteristics of a dietary pattern, like breakfast consumption, fast food intake, etc.

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The research strategy identified 58 papers which satisfied the inclusion criteria. Actually, with only three exceptions, all studies presented a cross-sectional design, which makes less reliable the assessment of an association with behavioral or health endpoints. The KIDMED index was used in the vast majority of the eligible studies, with a growing

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number of papers being published after the original study (2004)15 up to present. The KIDMED, which is a simple and easy tool to evaluate MD adherence, has initially been pro-

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posed as a questionnaire, but in several papers data were obtained using FFQs (Table 1). No results are available in the literature comparing these two different approaches. Conversely, MDS has been used in a relatively small number of papers and in several versions, which differed, even to a quite large extent, with respect not only to items, scoring systems and cut-off values, but also to the definition on what is detrimental and what is protective in a healthy diet (for example, dairy products). Moreover, categorization criteria varied between studies depending on the distribution of values for each MDS component in that particular study. As a last point, it should be reminded that KIDMED index has exclusively been used in the Mediterranean countries and MDS has been applied in both Mediterranean and non13

ACCEPTED MANUSCRIPT Mediterranean countries, while in 2 papers20,21 MD adherence was compared by different methods in the same cohorts of children (2-9 years) from 8 different European countries (Sweden, Germany, Hungary, Italy, Cyprus, Spain, Belgium and Estonia). EVALUATION OF ADHERENCE TO MD

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A recent narrative review suggested that MD adherence was poor in children and adolescents living in the Mediterranean countries83. Actually, data on MD adherence in the first two decades of life have mainly been provided by studies using the KIDMED index. Our systematic review shows that MD adherence, as estimated in such a way, widely varied in the Mediter-

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ranean countries for both children and adolescents (Table 2). The least prevalence of subjects with low MD adherence (<10%) and the greater prevalence of those with high adherence were frequently observed in some Spanish studies15,39,43,47,65,67.

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There is no clear and immediate explanation for the wide variations in MD adherence even within the same country, which might only partially be due to some factors such as gender, age, SES, etc. (see below). As far as methodological problems are concerned, it should be noted that a high heterogeneity of studies emerged in terms of subject characteristics, experimental protocols and different administration methodologies (telephone vs. vis a vis, interview vs. self-administration, questionnaire vs. FFQ) used to collect data.

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As already mentioned, MD adherence was also assessed in 14 studies using MDS (Table 2). Because of the differences between the various versions of that index, the papers cannot reasonably be compared with each other; in addition, the different components of MDS were

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analyzed by considering internal reference values and therefore results were highly dependent on the specific characteristics of the subjects participating in the study. Finally, in a comparison between different countries carried out by Tognon et al. in two dif-

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ferent studies20,21, MD adherence was significantly affected by the different methodology applied, i.e. the Swedish children with high adherence were 56.7% using fMDS vs. 37.6% using MDS, while the corresponding values for the Italian children with high adherence were 37.5% vs. 49.3% (Table 2). FACTORS ASSOCIATED WITH MD ADHERENCE We identified papers which took into consideration gender, age, SES and urbanization as potential determinants of MD adherence, as also suggested by a recent narrative review83. As gender is an important category of social differentiation, being aware of the differences between males and females is the first step to target successful interventions. Consistent find14

ACCEPTED MANUSCRIPT ings from the literature have indicated that in modern Western societies women often tend to have better dietary habits than men84. On the contrary, only in 7/33 of the studies included in this review females adhered to the MD significantly more than males. This result is in agreement with a recent review on MD adherence in Greek and Cypriot adult populations, reporting no difference between genders in most studies85.

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As major physical and psychological changes occur in the first two decades of life, recognizing changes in health behavior over this period is needed to promote young people’s health. For example, a recent review by Moreno et al.86 confirmed that the diet of adolescents in Europe is characterized by unsatisfactory food intakes, especially with respect to fruit and vege-

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tables, sugar-sweetened beverages, sweets, and meat87. In this systematic review a unfavorable trend with age was observed only in 9 out of 24 studies, thus most studies did not support the idea that MD adherence extensively changes with age.

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Reducing socio-economic inequalities in health behavior is one of the key environmental and health challenges of the present time88, and has become a priority in most of the countries, in line with Horizon 2020, WHO and Europe’s new health policy89. Previous studies have already shown that diet adequacy is significantly affected by SES83,90. In agreement with that evidence, we found that 15 out of 20 studies providing appropriate data observed a signifi-

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cant correlation between MD adherence and SES, in most cases assessed with parental educational level.

Finally, urbanization, a social process strongly affecting lifestyle, has been correlated with the shift from a traditional diet to a Western diet (with parallel negative changes in body

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composition and PA habits), being considered one of the environmental factors associated with childhood obesity91. The results of our review indicate that this topic has been addressed

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only in few of the eligible papers, with unconvincing results. As a matter of fact, 3 out of the 6 studies evaluating the issue found a significant difference in MD adherence due to urbanization, weakly suggesting that living in rural areas may be associated with a more traditional diet.

ASSOCIATION BETWEEN MD ADHERENCE AND ANTHROPOMETRIC VARIABLES OR BODY COMPOSITION A role of MD in preventing overweight, obesity or abdominal adiposity has been suggested in adults by recent systematic reviews81,92,93. In partial contrast, our paper focusing on children and/or adolescents shows conflicting results, since only 10/26 papers reported an inverse association of MD adherence with BMI values or prevalence of overweight and obesi15

ACCEPTED MANUSCRIPT ty. Even less consistent results, provided by few studies, came out by analyzing the relationship with abdominal adiposity (as WC) or fat mass. On the other hand, in agreement with the evidence in adults, there are only 2 papers reporting the association between MD adherence and higher BMI or fat mass (Table 3). Overall, exploring the relationship between MD and overweight/obesity is complex. First of

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all, it should be underlined that the majority of the studies on the issue had a cross-sectional design, not allowing to infer causal relationships between MD adherence and anthropometric variables. With respect to the only two prospective studies available in the literature23,25, they did not report any association of BMI or WC with MD adherence. In addition, as far as we are acknowledged on, there is only one randomized intervention study in obese children and

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adolescents94 (not included in this systematic review since it did not use any adherence score), demonstrating that the MD positively affected BMI, glucose and lipid profile.

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Secondly, there are important methodological differences and limitations in the studies included. For example, nearly 9/26 studies used self-reported data. The relationship between MD and obesity status in the self-reported measurement studies could have been influenced by the fact that obese individuals are more likely to under-report their body weight95. Among the studies reporting an association between MD adherence and weight status only 6 out of

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13 studies used measured data. Among the studies reporting no association between MD adherence and weight status, 10 out 12 studies used measured data. ASSOCIATION BETWEEN MD ADHERENCE AND LIFESTYLE VARIABLES

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As recent studies suggest, the clustering of poor dietary behavior, low PA levels, and/or sedentary behavior, may increase the risk of excess body fat and negatively impact other health outcomes in children and adolescents96,97. MD is considered as a dietary pattern that contrib-

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ute to better health and quality of life98,99. This is the first systematic review examining the papers which focused on the association between MD adherence and lifestyle variables. In 21 studies evaluated in the present review, PA and/or sedentary behavior were assessed through validated questionnaires. Despite their subjective nature, these tools (for example, the international Physical Activity Questionnaire, IPAQ100) have demonstrated reliability and validity being the most appropriate for surveillance systems and surveys101. Overall, we found that several studies reported a positive association of MD adherence with high levels of PA or even more frequently with less time spent in sedentary behavior (Table 4). 16

ACCEPTED MANUSCRIPT ASSOCIATION BETWEEN MD ADHERENCE AND FOOD GROUPS OR NUTRIENT AND ENERGY INTAKE The MD has been associated with nutritional adequacy in adult population82. As observed in this review, the number of studies that assessed this issue is limited, focusing on different nutrients and food groups. Nonetheless, a high MD adherence was always associated with a

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positive note for healthy nutrient/food consumption and never to an unhealthy one. In particular, a few studies reported a positive association between MD adherence and high fiber intake, good MUFA:SFA ratio and low SFA intake (Table 5).

Regarding food groups, the positive association between MD adherence and fruit, vegetable,

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and fish consumption was observed in agreement with studies in adults82. Furthermore, a negative association between MD adherence and meat, salty snacks and sweets was found in

FINAL REMARKS AND CONCLUSIONS

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the pediatric studies which analyzed the “anti” Mediterranean foods (Table 5).

To the best of our knowledge, this is the first paper that has systematically reviewed the scientific literature available on MD adherence in children and adolescents. To make the review more effective and clear, we thoroughly examined the different MD adherence indexes in

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terms of number of items, question content, cut-off values, categorization criteria, etc. It should be noted that in most cases results were provided separately for children and adolescents, with all papers including both males and females. In addition, a large number of studies used the same index (KIDMED). Lastly, this is the first description of studies focusing on

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the association between MD adherence and lifestyle variables. Indeed, there are some limitations to our review. Adherence indexes could first have been

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developed for assessing diet quality and not for evaluating the association with a specific behavior or health endpoint, possibly being a less accurate tool in this regard102. In addition, the evaluation of the relationships between MD adherence and endpoints of interest, which was often not a primary research objective, was also affected by the cross-sectional design of nearly all studies. With regard to KIDMED, the variability of the results may be also due to the different administration methodologies used. Lastly, the use of self-reported anthropometric data could have biased the association between MD adherence and weight status. In summary, this review shows that the design of adherence indexes, which was based on scientific evidence and a priori recognized characteristics of MD, depended at least in part on subjective criteria, for example reflecting food habits of a country. Adherence indexes 17

ACCEPTED MANUSCRIPT have been used in epidemiological surveys, whereas their reliability in assessing diet quality in the single subject remains unknown. Although the KIDMED index has been commonly applied in the Mediterranean countries, studies cannot easily be compared with each other, or aggregated for analysis, because of differences in subjects’ characteristics and experimental protocol. In addition, for some of the issues of interest (for example, urbanization) we found

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only few studies providing appropriate results. Overall, eligible papers suggest that MD adherence, as assessed with specific indexes, might be associated with PA and sedentary behavior (and possibly with weight status and diet adequacy), while results are not consistent with respect to gender and age. Further validation of

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MD indexes in terms of reproducibility and consistency with the MD is needed. At the same time, more prospective cohort and intervention studies may better elucidate the relationships

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of MD adherence with behavioral and health outcomes.

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82. Castro-Quezada I, Roman-Vinas B, Serra-Majem L. The Mediterranean Diet and Nutritional Adequacy: A Review. Nutrients. 2014; 6: 231-248. Doi:10.3390/nu6010231. 83. Grosso G, Galvano F. Mediterranean diet adherence in children and adolescents in southern European countries. NFS Journal. 2016;3:13-19. 84. Arganini C, Saba A, Comitato R, Virgili F, Turrini A. Gender Differences in Food Choice and Dietary Intake in Modern Western Societies, Public Health - Social and Behavioral Health, Jay Maddock (Ed.), InTech, 2012. Available at: http://www.intechopen.com/books/public-health-social-and-behavioral-health/genderdifferences-in-foodchoice-and-dietary-intake-in-modern-western-societies. Accessed on May 16, 2012. 85. Kyriacou A, Evans JM, Economides N, Kyriacou A. Adherence to the Mediterranean diet by the Greek and Cypriot population: a systematic review. Eur J Public Health. 2015;25(6):1012-1018. 25

ACCEPTED MANUSCRIPT 86. Moreno L.A, Gottrand F, Huybrechts I, Ruiz JR, González-Gross M, DeHenauw S, for the HELENA Study Group. Nutrition and lifestyle in European adolescents: the HELENA (Healthy Lifestyle in Europe by Nutrition in Adolescence) study. Adv Nutr. 2014; 5:615S623S.

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87. World Health Organization. Set of Recommendations on the Marketing of Foods and Non-Alcoholic Beverages to Children. WHO. 2010. Geneva, Switzerland. Available at http://whqlibdoc.who.int/publications/2010/9789241500210_ eng.pdf

SC

88. World Health Organization. Parma Declaration on Environment and Health. Fifth Ministerial Conference on Environment and Health “Protecting children’s health in a changing environment”. 2010. Parma, 10-12 March. Available at: http://www.euro.who.int/__data/assets/pdf_file/0011/78608/E93618.pdf

M AN U

89. World Health Organization. Review of social determinants and the health divide in the WHO European Region: final report. UCL Institute of Health Equity. 2013 Copenhagen, Denmark. Available at http://www.euro.who.int/__data/assets/pdf_file/0004/251878/Reviewof-social-determinants-and-the-health-divide-in-the-WHO-European-Region-FINALREPORT.pdf?ua=1. 90. Darmon N, Drewnowsky A. Does social class predict diet quality? Am J Clin Nutr. 2008; 87: 1107-1117.

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91. Popkin BM. Urbanization, lifestyle changes and the nutrition transition. World Dev. 1999; 27: 1905–16. 92. García-Fernández E, Rico-Cabanas L, Rosgaard N, Estruch R, Bach-Faig A. Mediterranean diet and cardiodiabesity: a review. Nutrients. 2014;6:3474-3500.

EP

93. Grosso GI, Mistretta A, Frigiola A, et al. Mediterranean diet and cardiovascular risk factors: a systematic review. Crit Rev Food Sci Nutr. 2014;54(5):593-610. doi:10.1080/10408398.2011.596955.

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94. Velázquez-López L, Santiago-Díaz G, Nava-Hernández J, Muñoz-Torres AV, MedinaBravo P, Torres-Tamayo M. Mediterranean-style diet reduces metabolic syndrome components in obese children and adolescents with obesity. BMC Pediatr. 2014; 5:14:175. 95. Spencer EA, Appleby PN, Davey GK, Key TJ. Validity of self-reported height and weight in 4808 EPIC-Oxford participants. Public Health Nutr. 2002;5(4):561-565. 96. Gubbels JS, van Assema P, Kremers SP. Physical Activity, Sedentary Behavior, and Dietary Patterns among Children. Curr Nutr Rep. 2013;2(2):105-112. 97. Iaccarino Idelson P, Scalfi L, Vaino N, et al. Healthy behaviours and abdominal adiposity in adolescents from southern Italy. Public Health Nutr. 2014;17(2):353-360. 98. Vasto S, Barera A, Rizzo C, Di Carlo M, Caruso C, Panotopoulos G. Mediterranean diet and longevity: an example of nutraceuticals? Curr Vasc Pharmacol. 2014;12(5):735-738. 26

ACCEPTED MANUSCRIPT 99. Trovato GM. Behavior, nutrition and lifestyle in a comprehensive health and disease paradigm: skills and knowledge for a predictive, preventive and personalized medicine. PMA Journal. 2012; 3:8. 100. Craig C, Marshall AL, Sjostrom M, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003; 35: 1381-1395.

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101. Chinapaw MJ, Mokkink LB, van Poppel MN, van Mechelen W, Terwee CB. Physical activity questionnaires for youth: a systematic review of measurement properties. Sports Med. 2010;40:539-563.

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EP

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SC

102. Lazarou C, Newby PK. Use of dietary indexes among children in developed countries. Adv Nutr. 2011;2:295-303. doi: 10.3945/an.110.000166.

27

ACCEPTED MANUSCRIPT ACKNOWLEDGMENTS The three authors equally contributed to prepare the manuscript. P.I.I. and L.S. conceived the study and performed the database search. P.I.I. and G.V. wrote the first draft. All authors participated in data interpretation, data analysis and revision of the article. All the authors read and approved the final manuscript.

RI PT

Funding. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

AC C

EP

TE D

M AN U

SC

Declaration of interest. The authors have no relevant interests to declare.

28

ACCEPTED MANUSCRIPT

TE D

EP

AC C

McCourt et al. (2014)25

Monteagudo-Sanchez et al.(2012) Monjardino et al. (2014)23 Navarro-Solera et al.(2014)65 Noale et al. (2014)33 Ozen et al. (2015)34 Papadaki et al. (2015)66 Perez Gallardo et al. (2011)67 Roccaldo et al. (2014)24 Sahingoz et al. (2011)68

37

29

1015

A

847 1180 777 565 1961 525 350 1740 890

C A C+A A A A C C A

Study design

RI PT

A A A A A A A C C+A A A A C A A A C C+A A A A A C C+A C+A C+A C+A C+A C+A A A A C+A C+A A A

MD adherence scoring system

Age

Greece Spain Greece Greece Spain Spain Greece Spain Greece Greece Greece Portugal Mexico Spain Spain Greece Greece Spain Spain Spain Greece Italy UK Greece Greece Cyprus Cyprus Cyprus Cyprus Spain Greece Greece Spain Spain Spain Greece Northern Ireland Spain Portugal Spain Italy Spain Greece Spain Italy Turkey

M AN U

Antonogeorgos et al. (2013)38 Arriscado et al. (2014)39 Arvaniti et al. (2011)40 Arvaniti et al. (2011)41 Asensi et al. (2015)42 Ayechu et al.(2010)43 Bargiota et al. (2013)44 Castro-Rodriguez et al. (2008)26 Chatzi et al. (2007)22 Costarelli et al. (2013)45 Costarelli et al. (2013)46 Da Rocha Leal et al. (2011)47 De Battle et al. (2008)27 del Mar Bibiloni et al. (2011)36 del Mar Bibiloni et al. (2012)48 Farajian et al. (2011)49 Garcia-Marcos et al. (2007)28 Gonzales Barcalà et al. (2010)29 Grao-Cruces et al. (2013)50 Grao-Cruces et al. (2014)51 Grigoropoulou et al. (2011)52 Grosso et al. (2013)53 Jennings et al. (2011)30 Kontogianni et al. (2008)54 Kontogianni et al. (2010)55 Lazarou et al. (2009)56 Lazarou et al.(2009)57 Lazarou et al. (2009)58 Lazarou et al. (2010)59 López et al.(2013)60 Lydakis et al. (2012)61 Magriplis et al. (2011)62 Mariscal-Arcas et al. (2009)63 Mariscal-Arcas et al. (2010)31 Martinez et al. (2010)32 Mazaraki et al. (2011)64

KIDMED-Q KIDMED-Q KIDMED-FFQ KIDMED-FFQ KIDMED-Q KIDMED-Q KIDMED-Q MDS KIDMED-FFQ* KIDMED-Q KIDMED-Q KIDMED-Q MDS MDS KIDMED-FFQ KIDMED-FFQ MDS MDS KIDMED-Q KIDMED-Q KIDMED-FFQ KIDMED-FFQ MDS KIDMED-Q KIDMED-Q KIDMED-FFQ KIDMED-FFQ KIDMED-FFQ KIDMED-FFQ KIDMED-Q KIDMED-Q KIDMED-FFQ KIDMED-FFQ MDS MDS KIDMED-Q MDS

CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS, P

T-MDS KIDMED-FFQ* KIDMED-Q MDS MDS KIDMED-Q KIDMED-Q KIDMED-FFQ* KIDMED-Q

CS CS, P CS CS CS CS CS CS CS

SC

Sample size 1125 321 700 700 379 1956 382 1784 690 359 391 390 1476 362 1961 4786 20106 14745 1973 19888 1125 1136 1700 1305 1305 1140 1140 1140 1140 800 277 4580 3190 3190 1231 365

Country

Reference

Table 1 Main characteristics of the included studies

ACCEPTED MANUSCRIPT

Tognon et al. (2014)

21

Tsartsali et al. (2009)74 Tsioufis et al. (2009)75 Vassiloudis et al. (2014)76

1127 517 2513 2513 3166 3850 2062

A A A A C+A C+A C

7940

C

KIDMED-Q MDS KIDMED-Q KIDMED-Q KIDMED-Q KIDMED-Q KIDMED-Q MDS

fMDS

14972

C

200 498 528

A A A

CS CS CS CS CS CS CS CS

RI PT

Tognon et al. (2014)20

Italy Portugal Spain Spain Spain Spain Spain 8 European countries 8 European countries Greece Greece Greece

KIDMED-Q KIDMED-FFQ KIDMED-Q

SC

Santomauro et al. (2014)69 Santos et al. (2014)35 Schröder et al. (2010)70 Schröder et al. (2013)71 Serra-Majem et al. (2003)72 Serra-Majem et al. (2004)15 Sotos-Prieto et al. (2015)73

CS, I

CS CS CS

AC C

EP

TE D

M AN U

* according to the criteria indicated by the authors. Abbreviations: A = adolescents; C = children; CS = cross-sectional; KIDMED-FFQ = index derived from a more detailed FFQ questionnaire; fMDS = food frequency Mediterranean Diet Score KIDMED-Q = index obtained from the 16-items KIDMED questionnaire; I = intervention; MD = Mediterranean Diet; MDS = different versions of the Mediterranean Diet Score; P = prospective.

30

ACCEPTED MANUSCRIPT Table 2 Adherence to the Mediterranean Diet according to the different methods.

Mean score

Categories

Asensi et al. (2015)42

8.5

-

0-12

-

4.7

0-12

4.6

-

0-12

-

30.4

0-12

5.8 M 6.0 F 5.6 R 5.8 U 5.8

15.6 R 14.7 U 17.2

0-12

-

6.7

0-12

-

M 52.0 F 50.0

0-10

-

0-12

6.3

0-12

-

0-12

3.6

0-12

-

M 6.3 F 6.1 R 5.3 U 4.7 R 5.8 U 4.8

0-12 0-12 0-12

48.6

46.7

-

-

59.0

10.6

64.1 R 67.2 U 59.7

20.3 R 18.8 U 23.1

50.4

42.9

M 41.0 F 50.0

M 7.0 F 11.0

27.9

43.8

28.3

-

-

-

7.2

50.8

42.1

46.8

48.9

4.3

R 8.8 U 13.1

R 55.7 U 57.2

R 35.5 U 29.7

-

-

-

-

-

-

R 18.1 U 27.2

R 70.1 U 64.0

R 11.8 U 8.8

0-12

-

3-12yrs 14.9 13-18yrs 27.0

3-12yrs 73.8 13-18yrs 68.6

3-12yrs 11.3 13-18yrs 8.3

0-12

NW 4.9 OW 4.5 OB 3.5

-

-

-

0-12

-

R 34.6 U 39.5

R 57.0 U 55.1

R 8.4 U 5.4

AC C

Kontogianni et al. (2010)55 Lazarou et al. (2009)57 Lazarou et al. (2009)58 Lazarou et al. (2010)59

-

-

EP

Kontogianni et al. (2008)54

Good (≥8)

0-12

TE D

Ayechu et al. (2010)43 Bargiota et al. (2013)44 Chatzi et al.a (2007)22 Costarelli et al. (2013)45 Da Rocha Leal et al. (2011)47 Farajian et al. (2011)49 Grao-Cruces et al. (2013)50 Grao-Cruces et al. (2014)51 Grigoropoulou et al. (2011)52 Grosso et al. (2013)53

Average (4-7)

M AN U

Antonogeorgos et al. (2013)38 Arriscado et al. (2014)39 Arvaniti et al. (2011)40 Arvaniti et al. (2011)41

Poor (≤3)

RI PT

KIDMED

SC

Score (minmax)

Method

López et al. (2013)60

Lydakis et al. (2012)61 Magriplis et al. (2011)62 Mariscal-Arcas et al. (2009)63 Mazaraki et al. (2011)64

0-12

-

37.3

55.9

6.8

NW 40.7 OW/OB 37.8 22.3 M 19.6 F 25.1

NW 52.4 OW/OB 60.3 52.9 M 55.0 F 50.6

NW 7.0 OW/OB 1.9 24.9 M 25.4 F 24.3

0-12

-

0-12

-

0-12

6.6

-

-

-

0-12

-

62.8

32.7

4.5

0-12

-

<10yrs 1.6 10-16yrs 2.0

<10yrs 49.5 10-16yrs 51.1

<10yrs 49.5 10-16yrs 46.9

0-12

-

41.9

51.2

6.8

-

-

-

16.6

30.1

53.3

Monjardino et al.a (2014)23

0-8

Navarro Solera et al (2014)65

0-12

M 5.2 F 5.1 7.07±4.46 M 7.01±4.51

31

ACCEPTED MANUSCRIPT F 7.13±4.41 M 5.8 F 5.5

M 15.4 F 19.6

M 61.1 F 61.1

M 23.6 F 19.3

0-12

7.6

2.1

43.9

53.9

0-10

-

32.8

62.2

5.0

0-12

-

17.9

59.2

22.9

0-12

-

23.0

60.5

16.5

0-12

Q1 (0-5) 22.6

Q2 (6-7) 22.5

Q3+Q4 (8-12) 53.6

Serra-Majem et al. (2004)15

0-12

4.2

49.4

46.4

Sotos-Prieto et al. (2015)73

0-12

-

-

28.0

12.5

52.1

6.0

51.9

43.7

-

0-12 0-12

59.5 4.0±2.2

41.9

0-12

4.4 Low (≤4)

Castro-Rodriguez et al. (2008)26 De Battle et al. (2008)27 del Mar Bibiloni et al.b (2011)36 Garcia-Marcos et al. (2007)28

Range 14-36

-

-

0-8

3.7±1.3

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

0-22

51.7±8.7% Median 50.8% Median 13; Range 4-20 12.0±2.3; Median 12; Range 4-20

TE D

0-22

Jennings et al. (2011)30 Mariscal-Arcas et al.b (2010)31

0-8

0-100

Martinez et al. (2010)32

4.1±1.6

62.7±11.3%; Median 62.8 57.9±8.9%; Median 57.3% Q1 52.7 %, Q4 62.8 %

EP

0-100

0-9

4.1±1.5

0-100

46.7%

AC C

McCourt et al. (2014)25 Monteagudo-Sanchez et al. (2012)37 Noale et al.c (2014)33

High (≥5)

0-22

0-100

Gonzales Barcalà et al. (2010)29

M AN U

MDS

SC

Tsartsali et al. (2009)74 Tsioufis et al. (2009)75 Vassiloudis et al. (2014)76

7.38±2.04

RI PT

0-12

Papadaki et al. (2015)66 Perez Gallardo et al. (2011)67 Roccaldo et al.a (2014)24 Sahingoz et al. (2011)68 Santomauro et al. (2014)69 Schröder et al. (2010)70

0-9

3.9±1.5

38.6

Ozen et al.b (2015)34

0-100

FFC 56.0%; non FFC 55.7%

-

-

Santos et al. (2014)35

0-9

51.3

48.7

0-7

During weekdays: Sweden 62.4; Estonia 67.0; Hungary 65.7; Belgium 64.5; Germany 70.6; Italy 50.7; Spain 65.7; Cyprus 70.4

During weekdays: Sweden 37.6; Estonia 33.0; Hungary 34.3; Belgium 35.5; Germany 29.4; Italy 49.3; Spain 34.3; Cyprus 29.6

Low (≤3)

High (>3)

Tognon et al. (2014)20

fMDS

32

47.4

14.0

ACCEPTED MANUSCRIPT Sweden 43.3; Estonia 73.7; Hungary 67.8; Belgium 67.3; Germany 64.9; Italy 62.5; Spain 68.2; Cyprus 75.8

Tognon et al. (2014)21

Sweden 56.7; Estonia 26.3; Hungary 32.2; Belgium 32.7; Germany 35.1; Italy 37.5; Spain 31.8; Cyprus 24.2

AC C

EP

TE D

M AN U

SC

RI PT

Scoring range: 0-8 o 0-9 references 25,27,30, 33; 0-22, references 26, 28, 29; 0-100 references 24, 31, 32, 36, 37. a modified versions of KIDMED b %Adherence > median value c MD adherence score: low <3; moderate 4-5; high 6-9 Abbreviations: F = females; FFC = Functional Food Consumers; M = Males; NW = Normal Weight; OW = Overweight; OB = Obese; Q1-Q4 = first to fourth quartile; R = Rural; U = Urban.

33

ACCEPTED MANUSCRIPT Table 3 Studies evaluating the association between adherence to the Mediterranean Di-

KIDMED

Measured

IOTF

-

KIDMED

Measured

IOTF

BIA

MDS

Reported by parents

IOTF

-

KIDMED

Measured

-

BIA

KIDMED

Reported by adolescents

MDS

Measured

IOTF

-

IOTF

BIA

IOTF

-

Reported by parents/ self KIDMED reported (adolescents)

Kontogianni et al. (2010)55

Reported by parents/ self KIDMED reported (adolescents)

IOTF

-

Lazarou et al. (2009)58

KIDMED

Reported by parents

IOTF

-

Reported by parents

IOTF

-

KIDMED

Measured

IOTF

-

Magriplis et al. (2011)62

KIDMED

Measured

IOTF

BIA

Mazaraki et al. (2011)64

KIDMED

Measured

IOTF

-

McCourt et al. (2014)25

MDS

Measured

-

-

KIDMED

Measured

-

-

Monjardino et al. (2014)23

EP

Lydakis et al. (2012)61

TE D

Kontogianni et al. (2008)54

Lazarou et al. (2010)59

KIDMED

Main results

TST, SST

RI PT

IOTF67

NS associations between adherence and BMI; % OW/OB, WC, % BF NS associations between adherence and BMI, % OW/OB NS associations between adherence and BMI, OW/OB; WC, WHtR, % BF Adherence differed between OB

SC

Body Composition

Measured

AC C

Jennings et al. (2011)30

KIDMED

and non-OB children both for boys and girls (p = 0.001).

NS association between adherence and BMI-SDS, % BF

M AN U

Grao-Cruces et al. (2013)50 Grosso et al. (2013)53

OW/OB Definition

Garcia-Marcos et al. (2007)28

Anthropometry

Arriscado et al. (2014)39 Arvaniti et al. (2011)40 Farajian et al. (2011)49

Scoring system

Reference

et and anthropometric and body composition variables.

34

High adherence protective from OB status (OR 0.59, 0.37-0.94)

NS association between adherence and BMI, BMI-SDS, WC, WHtR, and %BF NS association between adherence and BMI.

Lower adherence in OB adolescents but not in OB children. (p = 0.01) BMI negatively associated with KIDMED score (r=0.14, p=0.001) in the whole population Lower adherence only in OB girls but not in boys (p=0.023). Children with higher adherence less likely to be OW/OB (OR 0.20 , 95% confidence interval 0.04–0.98) Lower adherence in subjects with OB (p=0.044) or higher WC (p=0.039) compared with subjects with lower BMI or WC. NS association between adherence and BMI, %OW/OB and %BF. BMI and WC higher in adolescents with good KIDMED score than children with poor score (p<0.05). NS association between the change in MD adherence and the change in BMI and WC. NS association between adherence and BMI both at the baseline and after 4 year follow up.

ACCEPTED MANUSCRIPT Navarro Solera et al. (2014)65 Noale et al. (2014)33

KIDMED

MDS

Measured

WHOref

-

Significant association between adherence and OW/OB (p < 0.05) in the total sample and in females (p < 0.05)

Self reported

Cacciari et al.69

-

NS association between adherence and BMI.

WHO68

-

Self reported

IOTF

-

NS association between adherence and BMI.

Perez-Gallardo et al. KIDMED (2011)67

Measured

-

-

Negative correlation between adherence and BMI (r=-0.133; p<0.05).

Roccaldo et al. (2014)24

KIDMED

Measured

IOTF

-

Santomauro et al. (2014)69

KIDMED

Self reported

Schröder et al. (2010)70

KIDMED

fMDS

IOTF

-

-

-

Measured

IOTF

TST, SST

-

-

EP

Tognon et al. (2014)21

Measured

AC C

Tsartsali et al. (2009)74

KIDMED

Measured

SC

KIDMED

NS association between adherence and OW/OB. Poor adherence was significantly higher in UW students (35.9%) (p<0.05). Being NW or OW/OB seemed to be protective against poor adherence. BMI, WC and WHtR decreased across KIDMED quartiles (p=0.006; p=0.001; p=0.001 respectively). A 5-point increase in KIDMED score associated with a mean decline of 1.54 cm in sex-, age- and height-adjusted WC. At baseline: negative association between adherence and OW/OB (OR=0.85; 95%CI:0.77; 0.94), %BF (β=-0.22; 95%CI: -0.43; -0.01), and WC (β =-0.20; 95%CI: -0.46; 0.06). Intervention study: After 2 years, high adherence at baseline protected against increases in BMI z score (OR = 0.87, 95% CI: 0.78; 0.98), WC (OR = 0.87, 95% CI: 0.77; 0.98) and %BF (OR= 0.89, 95%CI:0.78; 1.00).

M AN U

Papadaki et al. (2015)66

TE D

Ozen et al. (2015)34

RI PT

Measured

UW functional food-consumers had higher risk to have low MD adherence; Non functional food-consumers adolescents were more likely to have low MD adherence.

MDS

NS association between adherence and BMI.

Abbreviations: BF = Body fat; BIA = Bioimpedance Analysis; BMI = Body Mass Index; BMI-SDS = BMI Standard Deviation Score; CI = Confidence Interval; fMDS = food frequency-based Mediterranean Diet Score; IOTF = International Obesity Task Force; MDS = Mediterranean Diet Score; NS = Not Significant; NW = Normal Weight; OB = Obese/Obesity; OR = Odds Ratio; OW = Overweight; SST = Subscapular Skinfold Thickness; TST = Triceps Skinfold Thickness; WC = Waist Circumference; WHO = World Health Organization; WHtR = Waist to Height Ratio; UW = Underweight.

35

ACCEPTED MANUSCRIPT Table 4 Studies evaluating the association between adherence to the Mediterranean Diet and lifestyle (physical activity and sedentary behavior). Main results

Arvaniti et al. (2011)41 del Mar Bibiloni et al. (2012)48

Magriplis et al. (2011)62 Martinez et al. (2010)32

Santomauro et al. (2014)69 Schröder el al. (2010)70

-

Good MD adherers were less sedentary than poor MD adherers (p<0.001).

M AN U

IPAQ94 score was higher in average MD adherers vs. poor MD adherers (p<0.001). Good MD adherers were more active than poor MD adherers (p<0.001). Adherence positively associated with PA (OR=1.19; 95%CI: 1.02-1.70). Higher adherence in children who practice MVPA ≥60 min/day (p=0.005).

-

-

NS association between adherence and LTPA.

Poor MD adherers spent more time on sedentary behavior (p=0.001).

-

Adherence negatively associated with screen exposure only in boys (p=0.038).

Better adherence in adolescents meeting the PA reccomandations versus those non meeting the reccomendations (p=0,007) Slightly higher IPAQ scores in average and good MD adherers (p=0.001). Lower MD adherence in sedentary adoLower adherence low active adolescents lescents (OR=2.66 95%CI: 0.92-7.68, p (OR=2.27; 95% CI: 1.27-4.81; p=0.033). =0.072 ). Positive association between adherence and Negative association between adhersports outside school (p<0.05). ence and TV viewing (p<0.05). Higher adherence in participants with higher PA scores (p=0.02). Positive association between adherence and PA frequency in girls (p=0.008). NS association between adherence and sport NS association between adherence and frequency. TV/PC.

AC C

Mazaraki et al. (2011)64 Mc Court et al. (2014)25 Monjardino et al. (2014)23 Noale et al. (2014)33 Ozen et al. (2015)34 Papadaki et al. (2015)66 Roccaldo et al. (2014)24

Negative association between adherence and media screen time (OR=1.77; 95%CI:1.08-2.91; p<0.05) in poor adherers vs. good adherers.

TE D

López et al. (2013)60

Higher adherence weakly associated with lower screen time (r=-0.30; p<0.01).

EP

Farajian et al. (2011)49 Grao-Cruces et al. (2013)50 Grosso et al. (2013)53 Jennings et al. (2011)30 Kontogianni et al. (2008)54 Lazarou et al. (2009)58

-

Sedentary Behavior

RI PT

Arriscado et al. (2014)39

Physical Activity Higher PA levels (p<0.001) and higher aerobic capacity (p=0.012) in children with good adherence. Higher adherence weakly associated with improved aerobic capacity (r=0.20; p<0.01) and higher PA levels (r=0.26; p<0.01). NS association between adherence and PA.

SC

Reference

No association between adherence and PA.

-

Negative association between adherence and inactivity (β= -1.19, p < 0.05).

Negative association between adherence and PC (β= - 1.162, p < 0.05).

Poor adherence in students who never played sports (OR=3.61, %95CI=2.05-6.35, p< 0.001)

Better adherence in children with lower screen time (TV/PC) (p<0.02) Poor adherence in students who spent > 3 hours in sedentary activity (OR=1.70, %95CI=1.11-2.59, p =0.015).

LTPA increased across KIDMED quartiles (p < 0.001) 36

ACCEPTED MANUSCRIPT Abbreviations: CI = Confidence Interval; IPAQ = International Physical Activity Questionnaire; LTPA = Leisure Time Physical Activity; MD = Mediterranean Diet; MVPA = Moderate-to-Vigorous-Physical-Activity; NS = Not Significant; OR = Odds Ratio; PA = physical activity; PC = personal computer; TV = television.

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Table 5 Studies evaluating the association between adherence to the Mediterranean Diet and food groups and nutrients.

Main results

Arvaniti et al. (2011)40

Slightly negative association between adherence and salty snacks consumption (p=0.02).

Grosso et al. (2013)53

Significant correlation between KIDMED score and SFA (p<0.001), CHO (p<0.001), fiber (p<0.001), sweets (p<0.001), fast foods (p<0.001), chips (p<0.05), soft drinks (p<0.001), fruit (p<0.001), vegetables (p<0.001), pasta (p<0.001), fish (p<0.001) and cheese (p<0.001).

Jennings et al. (2011)30

Higher energy intake in MDS fifth quintile than first quintile (p=0.005).

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Kontogianni et al. KIDMED scores were correlated with the intake of calcium (p<0.001), vitamin C (p<0.001) (2008)54 and fiber (p=0.010). Increased consumption across KIDMED categories for: dairy products (p<0.0001), poultry and rabbit (p=0.023), legumes (p<0.001), fish and seafood (p=0.001), nuts (p<0.001), bread (p<0.001), ready-to-eat cereals (p=0.002), whole-grain products (p=0.001), fruit (p<0.0001), Lazarou et al. leafy vegetables (p<0.0001), fresh legumes and seasonal vegetables (p=0.002), not fried pota58 (2009) toes (p=0.035), olives (p<0.0001), low glycemic index foods (p<0.0001), traditional Cypriot food (p=0.002) and unrefined foods increased across KIDMED categories. High MD adherers also reported higher intakes of refined foods and foods high in sugar. Magriplis et al. High sodium intake in children with average and good adherence (p<0.001). (2011)62 Adolescents with good adherence showed higher consumption of MD components (cereals and roots, vegetables, fruit, legumes, fish and MUFA:SFA ratio; p=0.001) and lower consumption of meat, whole milk and milk-products (p=0.003), and alcohol (p=0.0016).

Monjardino et al. (2014)23

Higher energy and calcium intake in the highest tertile of adherence (p<0.001).

Noale et al. (2014)33

Higher median values of CHO, fiber, Vitamins A, B6, C, D, folic acid, iron and MUFA (p<0.05) and less median values of SFA (p<0.001) and higher MUFA:SFA ratio (p<0.001) in higher MD adherers.

Ozen et al. (2015)34

Slightly higher adherence in functional food-consumers (p=NS).

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Martinez et al. (2010)32

Schröder et al. (2010)70 Schröder et al. (2013)71

Energy intake (p<0.001), proteins (p=0.002), and dietary fiber (p<0.001) increased across KIDMED quartiles. Fruit and vegetables (p<0.001), cereals (p=0.023), fish (p=0.001), and dairy products (p<0.001) increased across KIDMED quartiles, while meat (p=0.015), pastry and sweets (p<0.001). decreased. Poor adherence associated with high dietary energy density (p<0.001).

Higher consumption of fiber, calcium, iron, magnesium, potassium, phosphorus, and practically all the vitamins, with the exception of vitamin E, increased according to the KIDMED index (p<0.003 or less). Abbreviations: CHO = carbohydrates; MD = Mediterranean Diet; MDS = Mediterranean Diet Score; MUFA= Serra-Majem et al. (2003)72

Mono Unsaturated Fatty Acids; SFA=Saturated Fatty Acids.

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Figure 1 Flow chart summary of the search strategy

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Records identified through electronic search and screened (n=270)

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Identification/ screening

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Potentially relevant articles sought for full review (n=97)

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Records excluded (n=173)

Papers included in the review (n=58)

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Full text articles excluded (n=39): Subjects’ age (n=5) Low sample size (n=7) No adherence data (n=13) Not focusing on MD (n=2) Special populations (n=2) Reviews/commentaries/letters (n=10)

ACCEPTED MANUSCRIPT HIGHLIGHTS The KIDMED index was the most widely used scoring system.

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MD adherence widely varied in the Mediterranean countries.

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MD adherence was low in children and adolescents even in the Mediterranean countries.

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Most studies showed a positive association between MD adherence and physical activity and a negative association with sedentary behavior.

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Various studies showed a possible association between MD adherence and diet adequacy.

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