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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

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 70, respectively) and their 13-point MDA score (7 or <7, respectively).

Results:

Low HEI-score diets contained less (g/1000 kcal) 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/1000 kcal) 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 7 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.

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.

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 54 000 inhabitants, giving medical support to 150 000 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
figure1

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

Table 1 Detailed criteria taken into account in the 10-point HEI and 13-point MDA score

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 1000 kcal 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 2800 kcal29, 30 and the required servings.29, 31 Diets with HEI scores of 70(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 1 h 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 3500 r.p.m. for 5 min, 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 4.8 mUI/l, females 6.4 mUI/l), high-glucose (percentile 75th, males 81.25 mg/dl, females 82.5 mg/dl) and high HOMA-IR levels (percentile 75th, males 0.92, females 1.09), 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 4 mUI/l in insulinaemia with a power of 82 and 70% (nominal alpha=0.05) between neonates belonging to 70 and >70 HEI scores and <7 vs 7 MDA scores, respectively. A standard deviation of 3 and 1 for HOMA-IR and 6 and 2 mUI/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.

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 7 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 2 Maternal and neonatal variables in neonates belonging to total mothers and in those following an inadequate diet (HEI score 70) or an adequate diet (HEI score >70) or a low adherence to the mediterranean diet (MDA<7) or a high adherence (MDA 7)

Table 3 indicates that low HEI-score diets displayed lower (g/1000 kcal) 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 7 contained (per 1000 kcal) 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 3 Dietary energy, macronutrient and fatty acid energy contribution in the total of mothers and in those following an inadequate diet (HEI score 70) or an adequate diet (HEI score >70) or a low adherence to the mediterranean diet (MDA<7) or a high adherence (MDA 7)

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.

Table 4 Effect of selected possible confounders affecting the HOMA-IR, glucose and insulin neonatal levels

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 7 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
figure2

Number of neonates with low-normal (males <4.8 mUI/l, females <6.4 mUI/l) and high insulin cord-blood levels (males 4.8 mUI/l, females 6.4 mUI/l), low-normal (males <81.25 mg/dl, females <82.5 mg/dl) and high glucose cord-blood levels (males 81.25 mg/dl, females 82.5 mg/dl), and low-normal (males <0.92, females <1.09) and high HOMA-IR (males 0.92, females 1.09). (a) Neonates belonging to the dietary maternal HEI score (70 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, 7). 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.

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 1000 kcal, 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.

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 120 mg/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 7 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 1000 kcal 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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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.

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Correspondence to F J Sánchez-Muniz.

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

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Gesteiro, E., Rodríguez Bernal, B., Bastida, S. et al. 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. Eur J Clin Nutr 66, 1008–1015 (2012). https://doi.org/10.1038/ejcn.2012.92

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Keywords

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

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