Original Article

European Journal of Clinical Nutrition (2012) 66, 1008–1015; doi:10.1038/ejcn.2012.92; published online 25 July 2012

Maternal nutrition, infants and children

Maternal diets with low healthy eating index or mediterranean diet adherence scores are associated with high cord-blood insulin levels and insulin resistance markers at birth

E Gesteiro1, B Rodríguez Bernal2, S Bastida2 and F J Sánchez-Muniz2

  1. 1Servicio de Análisis Clínicos, Hospital de Mérida, Badajoz, Spain
  2. 2Departamento de Nutrición y Bromatología I (Nutrición), Facultad de Farmacia, Universidad Complutense de Madrid, Madrid, Spain

Correspondence: Professor FJ Sánchez-Muniz, Departamento de Nutrición y Bromatología I (Nutrición), Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal s/n, Madrid 28040, Spain. E-mail: frasan@farm.ucm.es

Received 6 June 2011; Revised 18 June 2012; Accepted 19 June 2012
Advance online publication 25 July 2012

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Abstract

Background/Objectives:

 

Few studies have used healthy eating index (HEI) and mediterranean diet adherence (MDA) scores to evaluate the diet quality during pregnancy. To determine the relationship between first trimester diet quality and insulin sensitivity/resistance biomarkers at birth.

Subjects/Methods:

 

Cord-blood insulin sensitivity/resistance biomarkers of the offspring of 35 women whose diets were ‘adequate’ or ‘inadequate’ according to their HEI score (>70 or less than or equal to70, respectively) and their 13-point MDA score (greater than or equal to7 or <7, respectively).

Results:

 

Low HEI-score diets contained less (g/1000kcal) carbohydrates (CHO; P=0.027) and fibre (P=0.011), and more fats (P<0.001) and cholesterol (P<0.001), and contributed (percentage contribution to total energy (%En)) fewer CHO (P=0.005), more fats (P=<0.001) and saturated fatty acid (SFA; P=0.002) than their high HEI-score counterparts. Low MDA-score diets contained less (g/1000kcal) fibre (P<0.001) and more cholesterol (P=0.05), had lower polyunsaturated fatty acids+monounsaturated fatty acid/SFA (PUFA+MUFA/SFA; P=0.05) and higher SFA/CHO (P=0.021) and ω-6/ω-3 PUFA ratios (P=0.044) than their respective counterparts. Women consuming the low HEI- or low MDA-score diets had low-fasting glycaemia (P=0.016 or P=0.025, respectively) but delivered infants with high insulinaemia (P=0.048 or P=0.017, respectively), homeostatic model assessment for insulin resistance (HOMA-IR; P=0.031 or P=0.049, respectively) and glycaemia (P=0.018 or P=0.048, respectively). The relative risk (RR) of high-neonatal glycaemia and insulinaemia were 7.6 (P=0.008) and 6.7 (P=0.017) for low vs high HEI-score groups. High HOMA-IR and high glucose RR were, respectively, 3.4 (P=0.043) and 3.9 (P=0.016) in neonates from the <7 MDA- vs greater than or equal to7 MDA-score group. These RRs were not affected by potential confounders.

Conclusion:

 

Maternal diets with low HEI- or MDA-scores during the first trimester of pregnancy negatively affect insulin resistance markers at birth.

Keywords:

pregnancy; neonates; HEI score; mediterranean diet adherence; insulin sensitivity/resistance markers

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Introduction

Diet during pregnancy is an important factor that affects maternal, fetal and infant health and wellbeing.1, 2 Food and energy-adjusted nutrient intakes from foods did not change appreciably from the first to the second trimester3 or from early to late pregnancy.4

The quantity and quality of dietary carbohydrates (CHO),5 dietary fibre6 and fats affect glucose metabolism and insulin resistance/sensitivity. Individuals with high-fat intake are more likely to develop glucose metabolism disorders than those who consume a low-fat diet.7, 8, 9 In addition, ω-3 polyunsaturated fatty acids (PUFA) and monounsaturated fatty acids (MUFA) affect insulin sensitivity/resistance and fasting plasma glucose levels in different population groups.7

The homeostatic model assessment for insulin resistance (HOMA-IR) has been widely used to evaluate the degree of insulin resistance in different populations.10, 11, 12 Our group has published the normal range for insulin resistance/sensitivity biomarkers at birth.13 HOMA-IR correlates with the saturated fatty acid/CHO (SFA/CHO) ratio,14, 15 suggesting that dietary quality greatly affects this insulin resistance biomarker. Kastorini et al.16 showed that the adherence to the mediterranean diet adherence (MDA) decreases the metabolic syndrome risk.

The healthy eating index (HEI) and the MDA scores have been largely employed to assess diet quality17 during pregnancy.18, 19, 20 HEI score reflects the complexity of dietary patterns18 and its validity has been demonstrated in studies using plasma biomarkers.21, 22 MDA score has been used to assess diet quality and its relationship with degenerative diseases.17, 23 PREDIMED, one large scale epidemiological study, uses the 14-point MDA score.24, 25 To our knowledge, there have been no studies on the possible association between diet quality during pregnancy, based on maternal HEI and MDA scores, and insulin sensitivity/resistance markers at birth.

Author’s hypothesis was that an ‘adequate’ diet (based on its HEI or MDA scores) during the first trimester of pregnancy results in lower values of insulin resistance biomarkers at birth than an ‘inadequate’ diet.

The aims of the current study were to analyse the quality of the maternal diet based on HEI and MDA scores during the first trimester of pregnancy and determine its influence on (a) maternal glycaemia and (b) insulin sensitivity/resistance biomarker levels in newborns. In addition, the authors compared the relative risk (RR) of displaying high-birth levels of glucose, insulin and HOMA-IR, and low values of the quantitative insulin sensitivity check index (QUICKI) between neonates whose mothers had consumed low HEI- or MDA-score diets in the first trimester of pregnancy and those whose mothers had followed adequate-score diets.

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Subjects and methods

Subjects

The subjects of the present study were 35 women who gave birth at the Mérida Hospital (Mérida, Extremadura, Spain), a regional hospital having 400 beds, placed in a town of approximately 54000 inhabitants, giving medical support to 150000 people. In all, 89 women were interested and contacted us through advertisements in the hospital. They were first informed about the study aims. A total of 23 future mothers were excluded. A total of 70 women completed the survey just before the first ultrasound pregnancy test at 12–15 week pregnancy, and were requested about their interest in performing an extra survey after delivery on major dietary changes occurring during the second and third trimesters. At weeks 24–28 of pregnancy, coinciding with their O’Sullivan glucose tolerance test,26 information about twin pregnancies and gestational diabetes was obtained. A total of 16 mothers were excluded. After delivery, a total of 35 women with their respective children were finally selected after excluding 19 mothers/neonates more. Exclusion factors in each stage of the study are summarized in Figure 1. After delivery, participant mothers were surveyed by telephone on major dietary changes occurring through second and third trimesters (Table 1). The participation rate was about 16% of participating women in the Mérida Cohort study. All infants studied were Caucasian: The study was performed in accordance with the Helsinki Declaration and approved by the Management and Ethical Committee of the Mérida Hospital.

Figure 1.
Figure 1 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Study flow diagram. Data obtained, recruited and exclusion reasons are detailed.

Full figure and legend (100K)


Methods

Dietary data collection
 

Participants, conducted by a trained dietician, completed a food frequency questionnaire (FFQ) that included 169 items classified according to food groups and based on FFQs used and validated in the enKid study.27 Photographs of sample portions were used to estimate the serving size and volumes consumed.28 The dietician reviewed together with the volunteer the usual consumption frequency of each food (per day/week/month), together with the normal food helping size, and specific information for mineral–vitamin supplements. Daily energy, nutrient intakes and HEI were calculated using a computer programme (DIAL, Madrid, Spain)29 to evaluate diet quality consumed during the first pregnancy trimester. Dietary data were adjusted to 1000kcal to reduce measurement error and to adjust for confounding. The HEI is based on a 10-component, 100-point scale and is a slight modification for the Spanish population of that of Kennedy et al.,18 taking into account recommended energy intakes of for 1600, 2200 and 2800kcal29, 30 and the required servings.29, 31 Diets with HEI scores of less than or equal to70(refs 18, 32) were labelled ‘inadequate’, whereas those with HEI scores of >70 were considered ‘adequate’.

The MDA score of 14 points used in the PREDIMED study24 was modified to 13-point MDA score taking into account that wine should be not consumed through the whole pregnancy. Each of the 13 components comprising the MDA score contributes a maximum of one point to the final score. An extra survey based on the 13 MDA points was performed to search on major dietary changes occurring during late pregnancy. Table 1 presents specific details considered in the surveys for HEI or MDA scores. Based on different studies32, 33 and considering that the average MDA score of the mothers was 6.87, and about 1/3 of them consumed diets with MDA score <7, the cutoff point for the MDA score <7 was selected to define low adherence to the mediterranean diet.

Maternal and neonatal data
 

Anthropometrical measurements were taken by trained personnel following hospital’s standard procedures. Data concerning mothers (age, gestational weight gain, O’Sullivan test basal and after 1h glycaemia, gestational diabetes, type of delivery, primarity/multiparity, education degree, place of residence) and neonates (weight, height, gender, gestational age, first and fifth minute Apgar indices) were obtained from hospital records. Data concerning of physical activity, seasonality, dietary habits and major dietary habits changes were obtained from the nutritional survey records.

Cord-blood measurements
 

After delivery, the umbilical cord was cut and arterial blood collected in BD Vacutainer SST II tubes (Becton Dickinson, Plymouth, UK). Blood was centrifuged at 3500r.p.m. for 5min, and serum aliquots frozen at −18°C until processed. Serum glucose and insulin were measured by the glucose hexokinase and electrochemiluminescence immunoassay (ECLIA) methods both supplied by Roche Diagnostics (Basel, Switzerland). Our laboratory is certified by AENOR and participates in the Spanish Clinical Chemistry Society (SEQC) External Quality Evaluation Program, which follows UNE-EN-ISO 9001:2000 standards. Intra-assay and inter-assay variation coefficients were 1% and 1.7% for glucose, 1.5% and 4.9% for insulin, respectively.

QUICKI, calculated by the formula 1/[(log insulin)(mIU/l)+(log glucose) mg/dl)];34 HOMA-IR, calculated as: glucose (mmol/l) × insulin(mIU/l)/22.5,35 and the glucose/insulin ratio were used as insulin sensitivity/resistance indices. The prevalence of neonates presenting high insulin, glucose and HOMA-IR, and low QUICKI values was calculated using Gesteiro et al.13 newborn reference data for high-insulin (percentile 75th, males greater than or equal to4.8mUI/l, females greater than or equal to6.4mUI/l), high-glucose (percentile 75th, males greater than or equal to81.25mg/dl, females greater than or equal to82.5mg/dl) and high HOMA-IR levels (percentile 75th, males greater than or equal to0.92, females greater than or equal to1.09), and low QUICKI levels (percentile 25th, males <0.39, females <0.37).

Statistics
 

Sample size was adequate to estimate absolute differences of 2.5 in HOMA-IR and 4mUI/l in insulinaemia with a power of 82 and 70% (nominal alpha=0.05) between neonates belonging to less than or equal to70 and >70 HEI scores and <7 vs greater than or equal to7 MDA scores, respectively. A standard deviation of 3 and 1 for HOMA-IR and 6 and 2mUI/l for insulin in neonates belonging to the low- and high-score diet groups, respectively, was assumed for this calculation. The Mann–Whitney U test was employed to compare diet characteristics and insulin sensitivity/resistance biomarkers in the different neonate groups. RR for neonates presenting high levels of glucose, insulin or HOMA-IR, or low QUICKI values in ‘inadequate’ vs ‘adequate’ diet groups and the exact one-tailed P-values for significant RR values (RR>1) were calculated. The effect of several confounders that could modify dietary habits and/or insulin sensitivity was also tested. The relationship between different parameters was obtained using the Spearman’s rank test. Statistical significance was set at P<0.05 using the SPSS (version 15.0) and the SAS (version 9.2) statistical software packages.

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Results

Table 2 shows that no significant differences were found between maternal and neonatal age, and anthropometric characteristics of groups classified according to the HEI and MDA score. Low HEI-score women had lower (P=0.016) glycaemia than their high HEI-score counterparts. Neonates whose mothers had consumed low HEI-score diets displayed significantly higher glycaemia (P=0.018), insulinaemia (P=0.048) and HOMA-IR (P=0.031) than those whose mothers had followed an ‘adequate’ diet. Women with MDA scores <7 had lower (P=0.025) glucose levels and weight gain during pregnancy (P=0.017) than their MDA greater than or equal to7 score counterparts. Neonates whose mothers followed low MDA-score diets had higher insulinaemia (P=0.017), glycaemia (P=0.048) and HOMA-IR (P=0.049) than neonates of mothers with adequate MDA diets. The mother or neonate distributions according to HEI or MDA score were not significantly affected by potential confounders.


Table 3 indicates that low HEI-score diets displayed lower (g/1000kcal) CHO (P=0.027) and fibre values (P=0.011) but higher fat (P<0.001) and cholesterol (P<0.001) levels, and SFA/CHO ratios (P<0.001) than the high HEI-score diets. Low HEI-score diets had higher contribution to total energy (%En) of fats (P<0.001) and SFA (P=0.002) and lower of CHO (P=0.005). Diets with MDA score <7 vs greater than or equal to7 contained (per 1000kcal) more (P<0.05) cholesterol but less fibre (P<0.001) and had higher SFA/CHO (P=0.021), ω6/ω3 (P=0.044) and lower PUFA+MUFA/SFA (P=0.05) ratios. The mother or neonate distributions according to HEI or MDA score were not significantly affected by most potential confounders.


Table 4 indicates that no significant effect can be attributable to seasonality, maternal dietary habits changes or other confounders on neonatal distribution according to HOMA-IR, glycaemia and insulinaemia.


MDA scores changed from 5.2±0.3 to 5.4±0.3 (P=0.083) and from 7.8±0.2 to 8.0±0.2 (P=0.102) from early to late pregnancy.

A high percentage of neonates whose mothers consumed low HEI- or MDA-score diets presented high insulinaemia, high glycaemia and high HOMA-IR (Figure 2). Compared with newborns at the ‘adequate’ HEI-score group, those belonging to the ‘inadequate’ diet presented a RR of 6.7 (P=0.017) for high insulinaemia, 7.6 (P=0.008) for high glycaemia and 2.9 (P=0.103) for high HOMA-IR values (Figure 2a). In comparison with the greater than or equal to7 MDA-score infants, the <7 MDA-score group presented a RR of 2.1 (P=0.177) for high insulinaemia, 3.9 (P=0.016) for high glycaemia and 3.4 (P=0.043) for high HOMA-IR levels (Figure 2b). RR appear adjusted for major potential confounders as distribution of neonates according to low-normal and high values for insulin resistance/sensitivity markers was not affected by confounders (Table 4).

Figure 2.
Figure 2 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Number of neonates with low-normal (males <4.8mUI/l, females <6.4mUI/l) and high insulin cord-blood levels (males greater than or equal to4.8mUI/l, females greater than or equal to6.4mUI/l), low-normal (males <81.25mg/dl, females <82.5mg/dl) and high glucose cord-blood levels (males greater than or equal to81.25mg/dl, females greater than or equal to82.5mg/dl), and low-normal (males <0.92, females <1.09) and high HOMA-IR (males greater than or equal to0.92, females greater than or equal to1.09). (a) Neonates belonging to the dietary maternal HEI score (less than or equal to70 or >70). The RR for high insulin level was 6.7 (P=0.017), for high glucose 7.6 (P=0.008) and for high HOMA-IR values 2.9 (P=0.103). (b) Neonates from the 13-point MDA score (<7, greater than or equal to7). RR for high insulin levels was 2.1 (P=0.177); for high glucose values, 3.9 (P=0.016); and for high HOMA-IR levels, 3.4 (P=0.043). For more methodological details see text.

Full figure and legend (51K)

HEI and MDA scores were significantly correlated (r=0.446; P=0.007). In all, 34.3% of mothers followed ‘adequate’ and 25.7% followed ‘inadequate’ diets according to both HEI and MDA scores. Both neonatal insulinaemia and HOMA-IR were inversely correlated with the HEI score (r=−0.365; P=0.031 and r=−0.363; P=0.032, respectively) and with the MDA score (r=0.357; P=0.048 and r=−0.338; P=0.047, respectively). Positive correlations, after adjusting data to 1000kcal, were observed between maternal dietary cholesterol and neonatal glycaemia (r=0.541; P<0.001), insulinaemia (r=0.431; P=0.010) and HOMA-IR (r=0.439; P=0.008); and between dietary fats and neonatal glycaemia (r=0.357; P=0.035). Dietary fats inversely correlated with QUICKI (r=−0.359; P=0.034) values.

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Discussion

Present data suggest for the first time that low HEI- or MDA-score maternal diets negatively affect neonatal insulin and HOMA-IR levels.

Epidemiological studies show that western-style diets can increase metabolic syndrome risk, whereas mediterranean-style diets have a protective role.25 During the first trimester of pregnancy, all the women participating in this study followed mediterranean-like diets but with a high contribution of meat and meat derivates and a moderate contribution of cereals and legumes, acceptable of vegetables and fruit and used olive oil as their principal oil for cooking and salads. The average HEI-score (mean (95% confidence intervals)) of the diets of the study participants was 67.5 (63.1–71.9), slightly below the cutoff point of 70 used by some authors to define good-quality diets.32 HEI scores in the present study were similar to those of Spanish women in general (73.7±10.5; mean±s.d.) and 25–44 year-old Spaniards (68.8±10.8).32 A large proportion (approximately 37%) of the participants of the current study displayed MDA scores <7.

Diet of the expectant mothers was similar to the present-day diet of Spaniards, with a high level of dietary fat and a relatively low contribution of CHO to total energy intake.36, 37 Although the energy contribution of SFA was high, the absolute and relative amounts of MUFA, ω-6, ω-3 and the ω-6/ω-3 ratio appear adequate according to current nutritional guidelines.20, 38

The maternal diet quality, as determined by HEI and MDA scores, significantly affected cord-blood insulin and HOMA-IR values. The smaller portions of vegetables, cereals, legumes and fruits consumed by women in the low HEI-score group explained their low CHO and fibre intakes. Dietary CHO quality and quantity are known to affect glycaemia and insulinaemia. The possible effect of glycemic load on insulin sensitivity markers should be tested in a larger number of pregnant mothers in future studies. Individuals with a high-fat intake (mainly as SFA) are especially prone to alterations of glucose tolerance and insulin sensitivity,7, 8, 9 as diets rich in SFA decreases the number of insulin receptors in most tissues. SFA selectively desensitize the response of peripheral tissue to insulin, whereas unsaturated fatty acids (PUFA+MUFA) may counteract this effect.39, 40 Such phenomena corroborate the close association between dietary fats and alterations in insulin secretion.41, 42

Both low HEI- and low MDA-score diets lagged far behind current European nutritional guidelines and recommendations31, 38 with regard to the energy contribution of fats, SFA and CHO and fibre content. In addition, ‘inadequate’ diets displayed SFA/CHO ratios that were approximately 50 and 22% higher than those of their high-score counterparts. These are important findings, as studies of isocaloric diets in which total fat represented 44 %En confirm that the SFA/CHO ratio is related to HOMA-IR14, 15 and that glucose tolerance was low in individuals consuming diets rich in SFA.8, 9 In addition, the ω6/ω3 ratio in the low MDA-score diets was 37% higher than in the high MDA-score diets, suggesting its impact on neonatal insulin and HOMA-IR levels. Martín de Santa Olalla et al.7 report that the ω6/ω3 ratio affects insulin resistance and sensitivity in certain population groups.

Although no clear evidence is yet available to explain why future mothers consuming high HEI- or MDA-score diets have higher basal glucose levels than their low-score counterparts, it appears that a high CHO intake during pregnancy induces high maternal glucose levels, permitting an adequate fetal glucose uptake. Differences between the diets consumed, as reflected through their HEI or MDA scores, do not appear to have any effect on maternal basal glucose at the O’Sullivan test, as none of the women studied presented fasting glycaemia greater than or equal to120mg/dl. However, certain neonatal insulin sensitivity/resistance biomarkers were significantly affected by maternal diet. Newborns at the low HEI-score group had 30% higher glycaemia; the insulinaemia and HOMA-IR were 2.5 and 4 times higher, respectively, than infants whose mothers consumed an ‘adequate’ diet. Similarly, newborns of mothers with <7 MDA-score diets presented HOMA-IR and insulin levels that were 5 and 3 times higher, respectively, than their greater than or equal to7 score counterparts. The beneficial effect of adherence to the mediterranean diet on HOMA-IR has been suggested.43 A high percentage of neonates belonging to the low HEI- or low MDA-score diets presented high insulinaemia, glycaemia and HOMA-IR, circumstance that was infrequent in their respective counterparts and explain the significant RR found. Dietary fats, and particularly those containing SFA, are known to increase insulin secretion44 and insulin resistance.45 Dietary fat unsaturation greatly influences β-cell function and insulin sensitivity under conditions of low-CHO intake.46 In addition, a western, low-CHO diet rich in SFA induced significantly higher insulin levels and lower cellular glucose uptake than a mediterranean or National Cholesterol Education Programme (NCEP)-step I diet.47 Previous epidemiological studies found high correlations between HOMA-IR values and dietary SFA/CHO ratios.14, 15 The lower consumption of fibre by mothers at low MDA- and HEI-score vs their respective high-score counterparts (20% and 30%, respectively) may, at least partially, explain present results as dietary fibre has been found to improve insulin sensitivity.6, 48

According to our data, after first trimester, except for fruits, fish/shellfish and sweets/pastries, non-remarkable changes occurred in of most food consumption (Supplementary Information). Crozier et al.4 reported that, in practical sense, women’s dietary patterns change little during pregnancy, although some differences were found for specific food groups.4

It has to be pointed out that present study shows some limitations, as the relatively low number of participating mothers, and the narrow range of neonatal bodyweights. The HEI and MDA scores cutoff points selected suggest acceptable or prudent diets but not optimum diets. Although the mediterranean diet characteristics are well defined, this is not a homogeneous dietary pattern. Timing of the FFQ would be a limitation as it was controlled only at early pregnancy. As the FFQ was completed by a trained dietician using food photographs, it should be accepted that the risk of potential errors due to lack of memory, and lack of precision with regard to food portions was lowered. In addition, dietary pattern showed minor changes during pregnancy. The effect of energy intake on dietary data should be discarded as diets were adjusted to 1000kcal to reduce measurement error. Confounder influences on the RR of neonatal insulin sensitivity/resistance biomarkers should be also discarded.

In conclusion, notwithstanding study limitations, our data indicate that poor diets, as determined by their HEI or MDA scores, negatively affect neonatal glucose homeostasis and, consequently, HOMA-IR values at birth. Further studies are needed to clarify these relationships and understand the impact that these neonatal values may have later in life.

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Conflict of interest

The authors declare no conflict of interest.

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References

  1. Rifas-Shiman SL, Rich-Edwards JW, Kleinman KP, Oken E, Gillman MW. Dietary quality during pregnancy varies by maternal characteristics in Project Viva: a US cohort. J Am Diet Assoc 2009; 109: 1004–1011. | Article | PubMed |
  2. Tsigga M, Filis V, Hatzopoulou K, Kotzamanidis C, Grammatikopoulou MG. Healthy eating index during pregnancy according to pre-gravid and gravid weight status. Public Health Nutr 2011; 14: 290–296. | Article | PubMed |
  3. Rifas-Shiman SL, Richard-Edwards JW, Willet WC, Kleinman KP, Oken E, Gillman MW. Changes in dietary intake from the first to the second trimester of pregnancy. Pediatr Perinat Epidemiol 2006; 20: 35–42. | Article |
  4. Crozier SR, Robinson SM, Godfrey KM, Cooper C, Inskip HM. Women’s dietary patterns change little from before to during pregnancy. J Nutr 2009; 139: 1956–1963. | Article | PubMed |
  5. Burger KNJ, Beulens JWJ, Boer JMA, Spijkerman AMW, van der A DL. Dietary glycemic load and glycemic index and risk of coronary heart disease and stroke in Dutch men and women: The EPIC-MORGEN Study. PLoS One 2011; 6: e25955. | Article | PubMed |
  6. Nillsson AC, Ostman WM, Knudsen KE, Holst JJ, Riörch IM. A cereal-based evening meal rich in indigestible carbohydrates increases plasma butyrate the next morning. J Nutr 2010; 140: 1932–1936. | Article | PubMed | ISI |
  7. Martín de Santa Olalla L, Sánchez-Muniz FJ, Vaquero MP. N-3 fatty acids in glucose metabolism and insulin sensitivity. Nutr Hosp 2009; 24: 113–127. | PubMed |
  8. Vessby B, Uusitupa M, Hermansen K, Riccardi G, Rivellese AA, Tapsell LC et al. Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU study. Diabetologia 2001; 44: 312–319. | Article | PubMed | ISI | CAS |
  9. Vessby B, Gustafsson IB, Boberg J, Karlström B, Lithell H, Werner I. Substituting polyunsaturated for saturated fat as a single change in a Swedish diet: effects on serum lipoprotein metabolism and glucose tolerance in patients with hyperlipoproteinaemia. Eur J Clin Invest 1980; 10: 193–202. | Article | PubMed |
  10. Jeppesen J, Hansen TW, Rasmussen S, Ibsen H, Torp-Pedersen C, Madsbad S. Insulin resistance, the metabolic syndrome, and risk of incident cardiovascular disease. A population-based study. J Am Coll Cardiol 2007; 49: 2112–2119. | Article | PubMed | ISI | CAS |
  11. Lemos JO, Rondo PHC, Pereira JA, Oliveira RG, Freire MBS, Sonsin PB. The relationship between birth weight and insulin resistance in childhood. Br J Nutr 2010; 103: 386–392. | Article | PubMed |
  12. Mericq V, Ong KK, Bazaes R, Peña V, Avila A, Salazar T et al. Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children. Diabetologia 2005; 48: 2609–2614. | Article | PubMed | ISI | CAS |
  13. Gesteiro E, Bastida S, Sánchez-Muniz FJ. Insulin resistance markers in term, normoweight neonates. The Merida cohort. Eur J Pediatr 2009; 168: 281–288. | Article | PubMed |
  14. Smith CE, Arnett DK, Corella D, Tsai MY, Lai CQ, Parnell LD et al. Perilipin polymorphism interacts with saturated fat and carbohydrates to modulate insulin resistance. Nutr Metab Cardiovasc Dis 2012; 22: 449–455. | Article | PubMed |
  15. Cabello-Saavedra E, Bes-Rastrollo M, Martinez JA, Diez-Espino J, Buil-Cosiales P, Serrano-Martinez M et al. Macronutrient intake and metabolic syndrome in subjects at high cardiovascular risk. Ann Nutr Metab 2010; 56: 152–159. | Article | PubMed |
  16. Kastorini C-M, Milionis HJ, Esposito K, Giugliano D, Goudevenos JA, Panagiotakos DB. The effect of mediterranean diet on metabolic syndrome and its components. J Am Coll Cardiol 2011; 57: 1299–1313. | Article | PubMed | ISI | CAS |
  17. Koning L de, Chiuve SE, Fung TT, Willett WC, Rimm EB, Hu FB. Diet-quality scores and the risk of type 2 diabetes in men. Diabetes Care 2011; 34: 1150–1156. | Article | PubMed |
  18. Kennedy ET, Ohls J, Carlson S, Fleming K. The healthy eating index: design and applications. J Am Diet Assoc 1995; 95: 1103–1108. | Article | PubMed | ISI | CAS |
  19. Mc Cullough ML, Feskanich D, Stampfer MJ, Giovannucci EL, Rimm EB, Hu FB et al. Diet quality and major chronic disease risk in men and women: moving toward improved dietary guidance. Am J Clin Nutr 2002; 76: 1261–1271. | PubMed | ISI | CAS |
  20. Bodnar LM, Siega-Riz AM. A diet quality index for pregnancy detects variation in diet and difference by sociodemographic factors. Public Health Nutr 2002; 5: 801–809. | Article | PubMed |
  21. Hahn CS, Rock CL, King I, Drewnowski A. Validation of the healthy eating index with use of plasma biomarkers in a clinical sample of women. Am J Clin Nutr 2001; 74: 479–489. | PubMed |
  22. Weinstein SJ, Vogt TM, Gerrior SA. Healthy eating index scores are associated with blood nutrient concentrations in the third National Health and Nutrition Examination Survey. J Am Diet Assoc 2004; 104: 576–584. | Article | PubMed | CAS |
  23. Trichopoulou A, Costacou T, Bamia C, Trichopoulos D. Adherence to a mediterranean diet and survival in a Greek population. N Engl J Med 2003; 348: 2599–2608. | Article | PubMed | ISI |
  24. Estruch R, Martínez-González MA, Corella D, Salas-Salvadó J, Ruiz-Gutiérrez V, Covas MI et alPREDIMED Study InvestigatorsEffects of a mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 2006; 145: 1–11. | PubMed | ISI |
  25. Salas-Salvado J, Fernandez-Ballart J, Ros E, Martinez-Gonzalez M-A, Fito M, Estruch R et alPREDIMED Study InvestigatorsEffect of a mediterranean diet supplemented with nuts on metabolic syndrome status. One-year results of the PREDIMED randomized trial. Arch Intern Med 2008; 168: 2449–2458. | Article | PubMed |
  26. O’Sullivan BA, Henderson ST, Davis JM. Gestational diabetes. J Am Pharm Assoc (Wash) 1998; 38: 364–371. , quiz 372-373. | PubMed |
  27. Serra Majem L, Aranceta Bartrina J. Alimentación infantil y juvenil. Estudio enKid. Ed, Masson: Barcelona, 2002.
  28. Mataix Verdú J, Llopis González J Jiménez Contreras JF, Lendoiro Otero RM, Meniño Olivera MJ (eds).. Manual gráfico e contenido nutricional de pratos galegos. Graphic Manual and Nutritional Content of Galicia Dishes. Consellería de Sanidad, Carrefour: Galicia, Spain, 1993.
  29. Ortega RM, López-Sobaler AM, Andrés P, Requejo AM, Aparicio A, Molinero LM. DIAL software for assessing diets and food calculations. Departamento de Nutrición (UCM) and Alce Ingeniería SA Madrid 2004: http://www.alceingenieria.net/nutricion.htm. (accessed April 2011).
  30. Requejo AM, Ortega RMEl rombo de la alimentación. Ministerio de Sanidad y Consumo: Madrid, 1996.
  31. Sociedad Española de Nutrición ComunitariaGuía de la alimentación saludable. SENC: Madrid, 2004.
  32. Norte Navarro AI, Ortiz Moncada R. Spanish diet quality according to the healthy eating index. Nutr Hosp 2011; 26: 330–336. | PubMed |
  33. Schröder H, Vila J, Marrugat J, Covas MI. Low energy density diets are associated with favorable nutrient intake profile and adequacy in free-living elderly men and women. J Nutr 2008; 138: 1476–1481. | PubMed |
  34. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000; 85: 2402–2410. | Article | PubMed | ISI | CAS |
  35. Livesey G. A systematic review of the glycaemic response to foods and health. ILSI Europe workshop. Glycaemic response on health: Nice, France, 2006 pp 82–127.
  36. Serra Majem L, Ribas Barba L, Aranceta Bartrina J, Pérez Rodrigo C, Saavedra Santana P, Peña Quintana L. Obesidad infantil y juvenil en España. Resultados del Estudio enKid (1998-2000). Med Clin. Barc, 2003; 121: 725–732. | Article |
  37. Spanish National Nutrition Survey (Encuesta Española de Ingesta Dietética). http://www.aesan.msc.es/AESAN/docs/docs/notas_prensa/
    Presentacion_ENIDE.pdf
    (accessed April 2011).
  38. FAO/WHOThe Joint FAO/WHO expert consultation on fats and fatty acids in human nutrition. FAO food and nutrition paper 91. Food and Agriculture Organization of the United Nations: Rome, 2010 ISSN 0254-4725.
  39. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003; 52: 726–733. | Article | PubMed | CAS |
  40. Roche HM. Fatty acids and the metabolic syndrome. Proc Nutr Soc 2005; 64: 23–29. | Article | PubMed | ISI |
  41. Meyer KA, Kushi LH, Jacobs DR, Folsom AR. Dietary fat and incidence of type 2 diabetes in older Iowa women. Diabetes Care 2001; 24: 1528–1535. | Article | PubMed | ISI | CAS |
  42. Salmeron J, Hu FB, Manson JE, Stampfer MJ, Colditz GA, Rimm EB et al. Dietary fat intake and risk of type 2 diabetes in women. Am J Clin Nutr 2001; 73: 1019–1026. | PubMed | CAS |
  43. Panagiotakos DB, Tzima N, Pitsavos C, Chrysohoou C, Zampelas A, Toussoulis D et al. The association between adherence to the mediterranean diet and fasting indices of glucose homeostasis: the ATTICA study. J Am Coll Nutr 2007; 26: 32–38. | PubMed |
  44. Holness MJ, Smith ND, Greenwood GK, Sugden MC. Acute ω-3 fatty acid enrichment selectively reverses high-saturated fat feeding-induced insulin hypersecretion but does not improve peripheral insulin resistance. Diabetes 2004; 53 (Suppl): S166–S171. | Article | PubMed |
  45. Mayer-Davis EJ, Monaco JH, Hoen HM, Carmichael S, Vitolins MZ, Rewers MJ et al. Dietary fat and insulin sensitivity in a triethnic population: the role of obesity. The insulin resistance atherosclerosis study (IRAS). Am J Clin Nutr 1997; 65: 79–87. | PubMed | CAS |
  46. López S, Bermúdez B, Pacheco YM, Villar J, Abia R, Muriana FJG. Distinctive postprandial modulation of β-cell function and insulin sensitivity by dietary fats: monounsaturated compared with saturated fatty acids. Am J Clin Nutr 2008; 88: 638–644. | PubMed |
  47. Pérez-Jiménez F, López Miranda J, Pinillos D, Velasco MJ, Castro P, Ostos M. A high MUFA and NCEP diet decrease the insulin resistance in young healthy subjects. Circulation 1998; 90: 193S.
  48. Lairon D. Dietary fibres: effects on lipid metabolism and mechanisms of action. Eur J Clin Nutr 1996; 50: 125–133. | PubMed | ISI | CAS |
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Acknowledgements

This study was partially supported by the Spanish AGL-2008 04892-C03–02 project. We thank the Gynecology and Obstetrics Department and Laboratory Services of Mérida Hospital (Extremadura, Spain), participant mothers and children, and Carmen Bravo from Departamento de Apoyo a la Investigación de la Universidad Complutense of Madrid.

Supplementary Information accompanies the paper on European Journal of Clinical Nutrition website

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