Carbohydrates, glycemic index and diabetes mellitus

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

Abstract

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 1 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.

Introduction

Childhood obesity has become a major public health issue, both for its increased prevalence worldwide, and its progression to major cardiovascular events later in life that further increases morbidity and mortality. As a disorder of energy balance, obesity is associated with insulin resistance and dyslipidemia. Different bioactive compounds in the diet are currently acknowledged to have favorable effects in these processes.1 Lignans are fiber-related phenolic compounds widely distributed in the diet2 as part of the dietary fiber complex.3 Lignans are especially abundant in grains, oilseeds, legumes and cruciferous vegetables.4, 5, 6 Six different lignans, that is, pinoresinol, lariciresinol, syringaresinol, medioresinol, matairesinol and secoisolariciresinol can be found at relevant concentrations in the human diet.7 These dietary lignans are absorbed, and to a certain extent (17%) excreted,8 although the major fraction undergoes an extensive metabolism by the gut microflora that results in the formation of the so-called enterolignans,9 attending to their colonic origin. These metabolites have been inversely associated with lower weight in women,10 and further with improved cardiovascular risk factors, and lower risks of acute cardiovascular events.11, 12, 13, 14, 15

There is no information on the intake of lignans in children and adolescents. The aim of this study was to determine the lignan intake and its dietary sources, and to further assess its association with prevalent obesity in a representative sample of Spanish children, adolescents and young adults.

Subjects and Methods

Study population

The enKid study design has been described in full elsewhere.16 Briefly, enKid is a population-based cross-sectional study conducted on a random sample of Spanish children, adolescents and young adults (2–24 years), between the years 1998 and 2000 (n=3534, 68.2% response rate). The study protocol was approved by the ethics committee of the Carlos III Health Institute (ISCIII) and the Spanish Society of Community Nutrition (SENC). Individual or parental consent (<18 years) was obtained for each participant.16 Dietary intake was assessed using 24-h diet recalls distributed evenly throughout the week and year to avoid weekly and seasonal variations in reporting. An additional 25% of the sample completed a second 24-h diet recall to further adjust the calculated intakes.16 The participants also completed a comprehensive questionnaire on demographic, socio-economic characteristics and lifestyle habits. The physical activity questionnaire was adapted from the CINDI program of the WHO and the questionnaire of the MARATHON study group for physical activity and leisure.17 Participant’s weight was measured on calibrated electronic scales, with an accuracy of ±100 g, and height was estimated using portable height boards Rolling Kawe model with an accuracy of ±1 mm, with participants standing barefoot and in standardized conditions, with the head located in the Frankfurt plane (horizontal plane between nose and ear canal). Age-adjusted body mass index was calculated according to Cole et al.18, 19 Body mass index cutoffs corresponded to those reported by the WHO, namely severe underweight (<18.50), normal weight (18.50–24.99), overweight (>=25.00) and obese (>=30.00). Age groups were defined as 2–5 years (preschool), 6–9 years (school), 10–13 (preadolescent), 14–17 years (adolescents) and 18–24 years (young adults). Complete data were obtained from a total of 3438 individuals.

Dietary lignan intake

The development of the Alignia database, an online-accessible compilation of values for lignans, has been described in detail elsewhere.6 The database contains information of 13 dietary lignans on 1390 different entries corresponding to 593 foods and beverages, and is publically available at www.alignia.org. A system for classification according to these quality scores was developed based on: analytical method in relation to the use of appropriate extraction techniques, reporting of validation parameters and limits of detection, number of samples and their origin and overall quality of the paper in which data were published.6 Food items from the Alignia database were extracted to match the enKid dietary assessment data set entries, and the lignan data with the highest quality score was selected for each entry. This ensured that most of the entries used to calculate intake contained complete information on individual lignans content, and that the most current and complete databases were considered.

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 within the data set explaining the intake of lignans. P-values in tables 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 parameters, the data set was divided in quartiles of lignan intake, and multivariate linear models with different degrees of adjustment were used. Model A was adjusted by age, income, population size and geographical location. Model B was further adjusted for total caloric intake, dietary fiber intake and physical activity. Interactions between dietary lignan intake and gender, and other variables of interest were also evaluated. All tests of statistical significance were two-sided and P-values below 0.05 were considered significant.

Results

Mean and interquartile range of dietary individual and total lignans are presented in Table 1. The median intake of the dietary lignans was 0.83 mg/day (interquartile range, 0.49–1.33 mg/day), corresponding mainly (37%) to pinoresinol. The lignans, secoisolariciresinol and matairesinol contributed only to 10% of the total lignan intake, consistently with previous reports addressing the importance of considering a broader range of lignans when assessing intake.23 The mean lignan intake was finally estimated to be 1.08 mg/day. The most important food sources of lignans (contribution >15%) were white bread (17%) and olive oil (16%). Other major contributors (>5%) were virgin olive oil (11%), whole-wheat bread (8%) and vegetables such as artichokes (5%), and to a lesser extent oranges (4%), lentils (3%) and coffee (3%). Dietary lignan intake was found significant and positively 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.

Table 1 Intake (mean, median and IQR, mg/day) of lignans in Spanish children and adolescents by individual compound

The intake of lignans by participant’s characteristics is presented in Table 2. No gender differences were found, but the intake was positively associated with age, varying from 0.61 mg/day in children aged between 2 and 5 years to 0.98 mg/day in young adults (18–24 years). The intake also varies significantly depending on the population size, with higher daily consumption in both rural (<10 000 inhabitants) and large cities (>350 000 inhabitants). By region, the highest intake is found in Northeast (1.05 mg/day) and South (0.89 mg/day) Spain. The lowest consumption corresponds to the Canary Islands (0.57 mg/day). No influence of the parental socio-economic status was found in the analysis. Intake was also significantly higher in those individuals with 2 h or more of weekly practice of sport (0.84 mg/day). 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 was significantly lower among children who practiced less than 60 min of activity (0.72 mg/day) and those who did it (0.84 mg/day).

Table 2 Median intake of lignans (mg/day) by participant’s characteristics

The association of lignan intake and obesity is presented in Table 3. A strong interaction in this association was found for gender, and therefore the results are presented in different strata. In model A, after adjusting for age, income, inhabitants and geographical location, no differences were found for girls and only marginal significance was found for boys on the highest quartile with odds ratio of 0.55 (95% confidence interval, 0.33–1.00). Model B was further adjusted by total energy intake, dietary fiber intake and physical activity level, but additional adjustment did not affect the association for girls. However for boys, a trend (P=0.025) towards lower prevalence of obesity with increasing intake of lignans was found. Comparing individuals on different quartiles of intake, a non-significant moderate decrease (odds ratio=0.76 (95% confidence interval, 0.38–1.54)) was found comparing the third versus the first quartile, but a strong association, with odds ratio of 0.34 (95% confidence interval, 0.17–0.70), was found for boys on the highest quartile of lignan intake.

Table 3 Adjusted odds ratios and 95% confidence intervals for obesity by quartiles of lignan intake, using conditional logistic regression models

Discussion

This is the first report on the consumption of lignans in children and adolescents, and therefore comparison with the intake in other studies is difficult. Previously calculated adult intake in countries such as Canada (0.85 mg/day),24 the United States (0.64 mg/day)25 and the Netherlands (1.24 mg/day),23 are within the ranges found in the present study. A similar figure was obtained for adults in Spain (0.76 mg/day) using household consumption data.6 In children, intake increases accordingly to age (Table 2) and the highest values are found for young adults (18–24 years). The literature on dietary lignan intake and body composition is scarce, and exclusive to adults. In previous studies, higher lignan dietary intake was found in individuals with lower body mass index,23 and lower total body fat as well as a better glucose disposal rate.26 High concentrations of plasma enterolignans have been also associated with body mass index.10, 27 These results are in agreement with this report, and show that dietary lignan intake is associated with lower prevalence of obesity. The main food determinants of dietary lignan intake in our study included traditional components of the Mediterranean diet, including olive oil (27% contribution, including virgin and refined olive oil), refined wheat bread (17%, whole-wheat bread (8%), vegetables (artichokes, 5%), fruits (orange, 4%) and legumes (lentils, 3%). The beverage that most contributed to lignan intake was coffee (3%).

It has been shown in previous studies that adherence to a Mediterranean dietary pattern seems to be associated with less obese populations.28, 29 In our study however, we found a gender-specific association that is difficult to explain. It has been hypothesized that lignan metabolism in humans could affect that of endogenous estradiol through competition to the estrogen receptors found on the major carriers, such as sex-hormone-binding globulin.30, 31 Lignans could therefore alter the estrogen levels available for hormone-dependent tissues, and by this effect influence the different estrogen-related physiological mechanism32 that take place during puberty. Finally, the additive and synergistic effects of other active phytochemicals found in the diet, may be partly responsible for the health benefits associated with vegetable-rich foods. Therefore, whether the association found in this report implies an active role of lignans on obesity development or can be merely used as an indicator of a healthier lifestyle deserves further attention.

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Acknowledgements

This study was financially supported by the Plan Nacional de I+D+i, SAF2008-01995, 2008–2011.

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Correspondence to J L Peñalvo.

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The authors declare no conflict of interest.

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Peñalvo, J., Moreno-Franco, B., Ribas-Barba, L. et al. Determinants of dietary lignan intake in a representative sample of young Spaniards: association with lower obesity prevalence among boys but not girls. Eur J Clin Nutr 66, 795–798 (2012). https://doi.org/10.1038/ejcn.2012.45

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Keywords

  • lignan
  • dietary intake
  • obesity
  • children

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