Determinants of Dietary Lignan Intake in a Representative Sample of Young Spaniards: Association with Lower Obesity Prevalence Among Boys but Not Girls

ORIGINAL ARTICLE Determinants of dietary lignan intake in a representative sample of young Spaniards: association with lower obesity prevalence among boys but not girls

JL Pen˜ alvo1, B Moreno-Franco1, L Ribas-Barba2 and L Serra-Majem2,3

BACKGROUND/OBJECTIVES: Lignan-rich diets have been associated with favorable health effects through improved metabolic profile. In this study, we hypothesized that dietary lignan intake could be also associated with childhood obesity. SUBJECTS/METHODS: We studied prevalent obesity in relation to lignan intake within the enKid study that involved 3438 children, adolescents and young adults (2–24 years old). Participant’s dietary records were used to calculate lignan dietary intake using a lignan composition database adapted to the Spanish diet. RESULTS: The mean intake of the dietary lignans was calculated as B1 mg/day, corresponding mainly (37%) to pinoresinol. No gender differences were found, but lignan intake was positively associated with age, physical activity level and dietary fiber intake, and negatively with the intake of polyunsaturated and saturated fatty acids. The main sources of dietary lignans were refined wheat, olive oil and whole-wheat bread. A strong association between dietary lignan intake and prevalent obesity was found only for boys, with odds ratio (highest versus lowest quartile of lignan intake) of 0.34 (95% confidence interval, 0.17–0.70) after adjusting for main confounders, including dietary fiber. CONCLUSIONS: Boys with the highest lignan-rich products including cereals, whole-grain products and olive oil, presented less cases of obesity in this representative sample of Spanish children and adolescents. It is unknown whether this association implies an active role of dietary lignans on obesity development, or is merely an indicator of a healthier lifestyle.

European Journal of Clinical Nutrition (2012) 66, 795–798; doi:10.1038/ejcn.2012.45; published online 16 May 2012 Keywords: lignan; dietary intake; obesity; children

INTRODUCTION with prevalent obesity in a representative sample of Spanish Childhood obesity has become a major public health issue, both children, adolescents and young adults. for its increased prevalence worldwide, and its progression to major cardiovascular events later in life that further increases SUBJECTS AND METHODS morbidity and mortality. As a disorder of energy balance, obesity Study population is associated with insulin resistance and dyslipidemia. Different The enKid study design has been described in full elsewhere.16 Briefly, bioactive compounds in the diet are currently acknowledged to enKid is a population-based cross-sectional study conducted on a random 1 have favorable effects in these processes. Lignans are fiber- sample of Spanish children, adolescents and young adults (2–24 years), related phenolic compounds widely distributed in the diet2 as part between the years 1998 and 2000 (n ¼ 3534, 68.2% response rate). The of the dietary fiber complex.3 Lignans are especially abundant study protocol was approved by the ethics committee of the Carlos III in grains, oilseeds, legumes and cruciferous vegetables.4–6 Six Health Institute (ISCIII) and the Spanish Society of Community Nutrition different lignans, that is, pinoresinol, lariciresinol, syringaresinol, (SENC). Individual or parental consent (o18 years) was obtained for each participant.16 Dietary intake was assessed using 24-h diet recalls medioresinol, matairesinol and secoisolariciresinol can be found at distributed evenly throughout the week and year to avoid weekly and relevant concentrations in the human diet.7 These dietary lignans 8 seasonal variations in reporting. An additional 25% of the sample are absorbed, and to a certain extent (17%) excreted, although completed a second 24-h diet recall to further adjust the calculated the major fraction undergoes an extensive metabolism by the intakes.16 The participants also completed a comprehensive questionnaire gut microflora that results in the formation of the so-called on demographic, socio-economic characteristics and lifestyle habits. The enterolignans,9 attending to their colonic origin. These meta- physical activity questionnaire was adapted from the CINDI program of the WHO and the questionnaire of the MARATHON study group for physical bolites have been inversely associated with lower weight in 17 women,10 and further with improved cardiovascular risk factors, activity and leisure. Participant’s weight was measured on calibrated 11–15 electronic scales, with an accuracy of ±100 g, and height was estimated and lower risks of acute cardiovascular events. using portable height boards Rolling Kawe model with an accuracy of There is no information on the intake of lignans in children and ±1 mm, with participants standing barefoot and in standardized adolescents. The aim of this study was to determine the lignan conditions, with the head located in the Frankfurt plane (horizontal intake and its dietary sources, and to further assess its association plane between nose and ear canal). Age-adjusted body mass index

1Area of Epidemiology and Population Genetics, Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain; 2Nutrition Research Foundation, University of Barcelona Science Park, Barcelona, Spain and 3Department of Clinical Sciences, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain. Correspondence: Dr JL Penãlvo, Epidemiology and Population Genetics, Centro Nacional de Investigaciones Cardiovasculares (CNIC), C/Melchor Fernańdez Almagro 3, Madrid 28029, Spain. E-mail: [email protected]. Received 7 February 2012; revised 4 April 2012; accepted 5 April 2012; published online 16 May 2012 Dietary lignans and prevalent obesity in Spanish children JL Penãlvo et al 796 was calculated according to Cole et al.18,19 Body mass index cutoffs (contribution 415%) were white bread (17%) and olive oil (16%). corresponded to those reported by the WHO, namely severe underweight Other major contributors (45%) were virgin olive oil (11%), (o18.50), normal weight (18.50–24.99), overweight (4 ¼ 25.00) and obese whole-wheat bread (8%) and vegetables such as artichokes (5%), (4 ¼ 30.00). Age groups were defined as 2–5 years (preschool), 6–9 years and to a lesser extent oranges (4%), lentils (3%) and coffee (3%). (school), 10–13 (preadolescent), 14–17 years (adolescents) and 18–24 years Dietary lignan intake was found significant and positively (young adults). Complete data were obtained from a total of 3438 individuals. associated with dietary fiber intake, and negatively with the intake of polyunsaturated and saturated fatty acids, and to a lesser extent, with carbohydrates and cholesterol. Dietary lignan intake The intake of lignans by participant’s characteristics is presented The development of the Alignia database, an online-accessible compilation 6 in Table 2. No gender differences were found, but the intake was of values for lignans, has been described in detail elsewhere. The positively associated with age, varying from 0.61 mg/day in database contains information of 13 dietary lignans on 1390 different entries corresponding to 593 foods and beverages, and is publically children aged between 2 and 5 years to 0.98 mg/day in young available at www.alignia.org. A system for classification according to these adults (18–24 years). The intake also varies significantly depending quality scores was developed based on: analytical method in relation to on the population size, with higher daily consumption in both the use of appropriate extraction techniques, reporting of validation rural (o10 000 inhabitants) and large cities (4350 000 inhabi- parameters and limits of detection, number of samples and their origin tants). By region, the highest intake is found in Northeast and overall quality of the paper in which data were published.6 Food items (1.05 mg/day) and South (0.89 mg/day) Spain. The lowest con- from the Alignia database were extracted to match the enKid dietary sumption corresponds to the Canary Islands (0.57 mg/day). No assessment data set entries, and the lignan data with the highest quality influence of the parental socio-economic status was found in the score was selected for each entry. This ensured that most of the entries analysis. Intake was also significantly higher in those individuals used to calculate intake contained complete information on individual lignans content, and that the most current and complete databases were with 2 h or more of weekly practice of sport (0.84 mg/day). considered. Similarly, we studied the consumption of lignan depending on the recommended practice of 60 or more min of moderate to vigorous physical activity daily, and also in this case, the intake Statistical methods All the statistical analyses were performed using the open-source statistical scripting language R version 2.13.0 (R Development Core Team).20 Non-normally distributed variables were log transformed for analysis. A stepwise linear regression analysis was used to determine the variables Table 2. Median intake of lignans (mg/day) by participant’s within the data set explaining the intake of lignans. P-values in tables characteristics correspond to the t-test comparison or F-tests for homogeneity of the means using the regTermTest function of the survey package.21,22 To evaluate the association between lignan intake and anthropometric Characteristic N Lignans (median, mg/day) P-value parameters, the data set was divided in quartiles of lignan intake, and Gender 0.995 multivariate linear models with different degrees of adjustment were used. Boys 1593 0.85 Model A was adjusted by age, income, population size and geographical Girls 1845 0.80 location. Model B was further adjusted for total caloric intake, dietary fiber intake and physical activity. Interactions between dietary lignan intake and Age (years) 0.001 gender, and other variables of interest were also evaluated. All tests of o 2–5 362 0.61 statistical significance were two-sided and P-values below 0.05 were 6–9 412 0.62 considered significant. 10–13 553 0.78 14–17 659 0.82 18–24 1452 0.98 RESULTS Mean and interquartile range of dietary individual and total Size (inhabitants) o0.001 lignans are presented in Table 1. The median intake of the dietary o10 000 704 0.89 lignans was 0.83 mg/day (interquartile range, 0.49–1.33 mg/day), 10 000–50 000 921 0.78 corresponding mainly (37%) to pinoresinol. The lignans, secoiso- 50 000–350 000 998 0.78 lariciresinol and matairesinol contributed only to 10% of the total 4350 000 815 0.88 lignan intake, consistently with previous reports addressing the Region 0.001 importance of considering a broader range of lignans when o 23 Center 771 0.79 assessing intake. The mean lignan intake was finally estimated to Northeast 887 1.05 be 1.08 mg/day. The most important food sources of lignans North 717 0.72 South 450 0.89 East 379 0.81 Canary Islands 234 0.57 Table 1. Intake (mean, median and IQR, mg/day) of lignans in Spanish children and adolescents by individual compound Social income 0.251 High 658 0.89 Lignan Mean (mg/day) Median (IQR) Medium 1053 0.80 Low 1537 0.82 Pinoresinol 0.45 0.31 (0.098–0.58) Siringaresinol 0.22 0.17 (0.093–0.29) Physical activity of at least moderate intensity (min/day) o0.001 Lariciresinol 0.14 0.11 (0.060–0.19) None 109 0.73 Secoisolariciresinol 0.18 0.075 (0.032–0.15) o60 1061 0.74 Enterolactone 0.014 0.013 (0.008–0.020) X60 2020 0.88 Medioresinol 0.017 0.009 (0.005–0.018) Matairesinol 0.016 0.008 (0.004–0.017) Sport practice activity (h/week) 0.001 Total lignans 1.08 0.83 (0.49–1.33) None 1445 0.79 o2 789 0.84 Abbreviation: IQR, interquartile range. X2 956 0.89

European Journal of Clinical Nutrition (2012) 795 – 798 & 2012 Macmillan Publishers Limited Dietary lignans and prevalent obesity in Spanish children JL Pen˜alvo et al 797 Table 3. Adjusted odds ratios and 95% conﬁdence intervals for obesity by quartiles of lignan intake, using conditional logistic regression models

Q1 Q2 Q3 Q4 P-trend

Girls Intake (mg/day) p0.46 0.47–0.80 0.81–1.31 X1.32 Obese/ non-obese 20/441 20/476 13/414 11/450 Adjusted model Aa 1.00 (ref) 0.95 (0.49–1.83) 1.26 (0.58–2.74) 1.07 (0.48–2.40) 0.647 Adjusted model Bb 1.00 (ref) 0.98 (0.49–1.95) 1.22 (0.49–2.52) 0.91 (0.37–2.22) 0.988

Boys Intake (mg/day) p0.51 0.52–0.86 0.87–1.34 X1.35 Obese/ non-obese 25/373 32/366 20/378 33/366 Adjusted model Aa 1.00 (ref) 0.68 (0.35–1.13) 1.01 (0.53–1.92) 0.55 (0.30–1.00) 0.310 Adjusted model Bb 1.00 (ref) 0.48 (0.25–0.89) 0.76 (0.38–1.54) 0.34 (0.17–0.70) 0.025 aAdjusted for age, income, population size and Spanish region. bFurther adjusted by total energy intake (Kcal/day), dietary fiber intake (g/day) and adherence to recommended physical activity. was significantly lower among children who practiced less than less obese populations.28,29 In our study however, we found a 60 min of activity (0.72 mg/day) and those who did it (0.84 mg/ gender-specific association that is difficult to explain. It has been day). hypothesized that lignan metabolism in humans could affect that The association of lignan intake and obesity is presented in of endogenous estradiol through competition to the estrogen Table 3. A strong interaction in this association was found for receptors found on the major carriers, such as sex-hormone- gender, and therefore the results are presented in different strata. binding globulin.30,31 Lignans could therefore alter the estrogen In model A, after adjusting for age, income, inhabitants and levels available for hormone-dependent tissues, and by this geographical location, no differences were found for girls and only effect influence the different estrogen-related physiological marginal significance was found for boys on the highest quartile mechanism32 that take place during puberty. Finally, the with odds ratio of 0.55 (95% confidence interval, 0.33–1.00). additive and synergistic effects of other active phytochemicals Model B was further adjusted by total energy intake, dietary fiber found in the diet, may be partly responsible for the health benefits intake and physical activity level, but additional adjustment did associated with vegetable-rich foods. Therefore, whether the not affect the association for girls. However for boys, a trend association found in this report implies an active role of lignans (P ¼ 0.025) towards lower prevalence of obesity with increasing on obesity development or can be merely used as an indicator intake of lignans was found. Comparing individuals on different of a healthier lifestyle deserves further attention. quartiles of intake, a non-significant moderate decrease (odds ratio ¼ 0.76 (95% confidence interval, 0.38–1.54)) was found comparing the third versus the first quartile, but a strong CONFLICT OF INTEREST association, with odds ratio of 0.34 (95% confidence interval, The authors declare no conflict of interest. 0.17–0.70), was found for boys on the highest quartile of lignan intake.

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European Journal of Clinical Nutrition (2012) 795 – 798 & 2012 Macmillan Publishers Limited