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Nutritional Epidemiology

Vegetable but Not Fruit Intake during Pregnancy Is Associated with Newborn Anthropometric Measures^1,2

³ CIBER en Epidemiología y Salud Pública, 08003 Barcelona, Spain; ⁴ Escuela Valenciana de Estudios para la Salud, Conselleria de Sanidad, 46017 Valencia, Spain; ⁵ Departamento de Salud Pública, Universidad Miguel Hernandez, 03203 Elche-Alicante, Spain; and ⁶ Hospital La Fe, 46009 Valencia, Spain

^* To whom correspondence should be addressed. E-mail: ballester_fer{at}gva.es.

	ABSTRACT

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
We examined the relationship between consumption of fruit and vegetables during pregnancy and anthropometric measures at birth in a general population mother-infant cohort in Valencia, Spain. A total of 787 infants born between May 2004 and February 2006 were included. Fruit and vegetable consumption during pregnancy was assessed by a FFQ administered using an in-person interview. We used multiple linear regression to assess associations between fruit and vegetable intake (in quintiles) and birth weight and length adjusted for sex and gestational age, and logistic regression to assess being small for gestational age (SGA) in weight and SGA in length, defined as adjusted birth weight or length below the 10th percentile. A linear relationship was found between vegetable consumption and having a SGA (weight) and SGA (length) baby. Women in the lowest quintile of vegetable intake during the first trimester had a higher odds of having a SGA (weight) baby than women in the highest quintile [odds ratio (OR), 3.7; 95% CI: 1.5–8.9; P-trend < 0.001] and had a higher odds of having an SGA (length) baby in the third trimester (OR, 5.5; 95% CI: 1.7–17.7; P-trend = 0.04) in multivariate analysis. We found a nonmonotonic relationship between adjusted birth weight and length and vegetable consumption during the first trimester; newborns in the 2 lowest quintiles of intake had a significantly lower weight and length than those in the 4th quintile. There was no association between fruit consumption and birth outcomes. Our findings indicate that vegetable consumption throughout pregnancy may have a beneficial effect on fetal growth.

	Introduction

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

One of the relevant nutritional factors during pregnancy is the intake of specific micronutrients such as folate, vitamin C, and carotenoids. These are plentiful in fruit and vegetables and have been associated with increased birth size within the full birth weight and birth length range in developed countries, where undernutrition is uncommon (10,11). Focusing on consumption of fruit and vegetables instead of the known specific micronutrients provided by them will enable other possible bioactive constituents of plants, such as phytochemicals, to be considered and will be valuable for nutritional counseling purposes. To our knowledge, only 2 studies, in very different populations of pregnant women, one from a rural area in India and the other in the general population in Denmark, have assessed the association of the intake of fruit and vegetables as a food group with birth size (12,13). Both studies found a small significant increase in birth weight with higher consumption of fruit and vegetables after adjustment for covariates.

In this study, our aim was to assess the association between fruit and vegetable consumption during pregnancy and anthropometric measures at birth in a general population mother-infant cohort in Valencia, Spain. We hypothesized that increased intake of fruit and vegetables would promote fetal growth.

	Materials and Methods

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
    Population and study design. As part of a multicentre project [Infancia y Medio Ambiente (INMA)]⁷ that aims to study the role of diet and environmental factors in fetal and infant health and development in different geographical areas of Spain, we set up a population-based birth cohort in a geographically defined area of the Valencian Community. Details about the research protocol have been published elsewhere (14).

Briefly, women from the study area who attended the first trimester prenatal population-based screening program for congenital malformations at the reference hospital (Hospital La Fe de Valencia) were eligible if they fulfilled the inclusion criteria (at least 16 y old, singleton pregnancy, inclusion visit at 10–13 wk, no assisted conception, no chronic hypertension, delivery foreseen at the reference hospital, and no communication handicap). From February 2004 to June 2005, 840 of the 1563 eligible women were included in the study after they signed the informed consent form (participation rate 54%). Fifteen women were recruited in October 2003 when a pilot study was conducted and they are also included in the analysis. Between inclusion in the study and delivery, 31 women had an abortion, 4 had a fetal death, 28 withdrew, and 5 were lost to follow up, leaving 787 pregnant women who delivered a live infant for the final analysis. Deliveries took place between May 2004 and February 2006. The Hospital La Fe Ethics Committee approved the research protocol.

    Assessment of fruit and vegetable intake. A semiquantitative FFQ was used to assess the usual dietary intake of 100 food items and beverages during the first and third trimesters. Participants were asked to report the frequency of consumption of 10 fruit items (oranges; orange juice; bananas; apples or pears; peaches, nectarines, or apricots; watermelon or melon; grapes; prunes or plums; kiwis; and olives) and 12 vegetable items (spinach; cabbage, cauliflower or broccoli; lettuce or endive; tomatoes; onions; carrots or squash; green beans; eggplant, zucchini, or cucumber; green, red, or yellow peppers; artichokes; asparagus; and garlic) during 2 different periods: the first trimester (10–13 wk) and third trimester (28–32 wk). The first FFQ collected information on average consumption of each item since the last menstrual period (LMP) and was given at 10–13 wk in 91.7% of the cases; the second FFQ was given at 28–32 wk in 84% of the cases and collected information on consumption during the period that had elapsed since the first FFQ was administered.

The 100-item FFQ is an expanded version of a previous 93-item FFQ similar to the Harvard questionnaire (15), which we validated and developed for an adult Spanish population in Valencia with a high proportion of women (16,17). Although the 100-item FFQ has not been validated in the pregnant women in our study, the validity and reproducibility of the 93-item FFQ was satisfactory when comparing the FFQ with 4 1-wk dietary records. The mean correlation coefficients for 1-y validity and reproducibility of nutrient intakes were 0.47 and 0.40, respectively (18).

Participants in our study were asked how often, on average, they had consumed each food item during the relevant study period. Standard units or serving sizes were specified for each food item in the FFQ. The questionnaire had 9 possible responses, ranging from "never or less than once per month" to "six or more times per day." The response for each food item was converted into average daily intake for each individual participant. The average daily intakes for each fruit and vegetable were added to give the total fruit and vegetable intake. Total energy intake was calculated from macronutrient and alcohol values, primarily obtained from food composition tables of the USDA (19). Caffeine (mg/d) and alcohol (g/d) intakes were assessed in the FFQ with specific items for coffee, nonalcoholic beverages, and other foods containing caffeine, wine, beer, and liquors, together with standard portions for all the items.

    Birth data ascertainment. Information on anthropometric measures at birth was obtained from the hospital delivery logs and medical records. Birth weight was measured by the midwife that attended the birth, whereas birth length was measured by a nurse when the newborn arrived in the hospital ward during the first 12 h. Gestational age was established on the basis of the date of the LMP self-reported by the mothers. An early ultrasound of the crown-rump length was also available and used for gestational dating when the difference from the LMP was 7 d. In 12.5% of the women, gestational age was estimated by ultrasound measurement.

Outcome variables were standardized birth weight (in g) and birth length (in cm) and small weight or length for gestational age. Birth weight and length were standardized for sex and gestational age (BWGA and BLGA) using the residual method. We defined small weight or length for gestational age (SGA) as a BWGA or BLGA below the 10th percentile based on growth reference charts standardized for both sex and gestational age for the Spanish population (20). Neither SGA (weight) nor SGA (length) could be defined for 1 newborn, because she was born very preterm and there was no value for her gestational age (23 wk) on the percentile charts.

    Other covariates and confounding factors. Potential confounding factors were selected from previously reported determinants of fetal growth in the biomedical literature. Information on sociodemographic and other potential confounding factors was collected during an interview at entry into the study and at the 3rd trimester using a structured questionnaire. BMI was calculated by dividing the self-reported weight before pregnancy in kg by the square of the height in meters. Total gestational weight gain was calculated as the product of gestational length in weeks and weekly maternal weight gain. The latter was previously adjusted for the last available gestational age to avoid the nonlinearity of weight gain during pregnancy. Both BMI and weight gain were further classified following the Institute of Medicine guidelines (21). Active prenatal smoking was defined as smoking at least 1 cigarette per day during 3rd trimester. Socioeconomic status was defined in 3 occupational categories according to current or most recent occupation, and for 12 women who were always housewives, according to the husband's occupation using a widely used Spanish adaptation of the British classification system (22). Social class I included managerial and senior technical staff and freelance professionals; class II included intermediate occupations and managers in commerce; class III included skilled nonmanual workers; class IV included skilled and partly skilled manual workers; and class V included unskilled manual workers. We used 3 categories (I+II, III, IV+V) in our analysis.

    Statistical analysis. We performed bivariate analysis to determine parental and infant characteristics associated with birth outcomes. Results are expressed as percentages or means ± SD in the text and tables for descriptive purposes. Unpaired Student's t tests and 1-factor ANOVA were used to compare the means of continuous variables and ² tests for categorical variables. Spearman correlation was used to estimate the correlation of fruit and vegetable intake between the 1st and 3rd trimesters. For continuous variables, we also checked for the shape of the relationship using graphical smoothing techniques (loess) (23). Height of both parents showed a linear relationship and was therefore included as a continuous variable in the models. The rest of the continuous variables were categorized to account for nonlinear associations. The loess fit for our explanatory variables, i.e. fruit and vegetable intake, gave a nonmonotonic shape for their relationship with anthropometric measures, especially in the case of fruit intake. Therefore, we examined the associations between birth outcomes and dietary exposure variables using quintiles of fruit and vegetable intake. Multiple linear regression was used to estimate the independent associations between continuous birth outcomes (BWGA and BLGA) and quintiles of fruit/vegetable intake adjusting for covariates. We included the fruit and vegetable variables in quintiles together with all the potential confounding factors in the same model. We then checked the change in R² for each covariate or confounding factor manually and retained it if it was related to the outcome (P < 0.20). We included maternal age and energy intake in quintiles in all models irrespective of their significance; we included energy intake in the models due to the correlation between food intake and energy intake (24). We also performed a sensitivity analysis using the fruit and vegetable intake variables adjusted for energy intake (24). For continuous outcome variables, when comparing differences among quintiles, using a different category reference than the one presented in the tables, results are expressed as means ± SEM in the text. For dichotomous birth outcomes (SGA), we used logistic regression analysis following the same strategy as for continuous data, using the likelihood ratio test (LRT) for exclusion or inclusion of covariates. P < 0.05 for the estimate of the effect was considered significant.

It has been reported that the association of fruit and vegetable intake during pregnancy with anthropometric measures at birth are stronger among lean women (12,13). It has also been reported that pregnant women who smoke may have lower plasma levels of antioxidant vitamins than do nonsmokers (25). Therefore, we investigated the possibility of effect modification with respect to prepregnancy weight and smoking status. The interaction terms were not significant for either prepregnancy weight or for smoking (P > 0.05).

We performed bivariate and multiple linear regression using the SPSS statistical software package, version 15 for Windows and logistic regression using the STATA version 9 statistical software package (Stata).

	Results

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
Mean maternal age was 30 y and ranged from 16 to 43 y. Fifty-five percent were primiparous. Approximately 11% of the women were from abroad. A large proportion of women (23%) smoked during pregnancy (Table 1). Furthermore, 67% of the mothers had completed secondary education and, at the end of the first trimester of gestation, 62% were employed. Prepregnancy BMI was between 19.8 and 26.0 in 61% of the mothers and 24% of them were overweight or obese. The majority of women lived in metropolitan or semiurban areas (49 and 36%, respectively).

The daily intake of fruit and vegetables in this study population was 293.0 ± 216.1 and 213.3 ± 121.0 g/d, respectively. The correlation between the first and third trimesters of fruit and vegetable intake was 0.43 and 0.55, respectively (Spearman correlation; P < 0.01; 2-sided) among participants who answered both FFQ (n = 775). Mean intake of vegetables did not differ in the 2 trimesters (mean 2.0 ± 4.4 g, P = 0.65), whereas there was a difference of –25.5 ± 8.9 g (P < 0.001) between first and third trimester fruit intake.

The daily intake and range per quintile of fruit and vegetable consumption during the first trimester according to birth outcomes is shown (Table 2). For bivariate analysis, increasing consumption of vegetables was associated with higher BWGA and BLGA, although mean weight and length in the highest quintile were somewhat lower than in the 4th quintile. There was a lower proportion of SGA (weight) infants per category increment. In the case of birth length, the highest proportion of SGA (length) was in the first quintile of vegetable consumption, whereas the smallest was in the third. There was no clear pattern with regard to increasing fruit consumption and birth weight, length, or SGA (weight), although the highest proportion of SGA (length) was in the lowest quintile.

In the adjusted analysis, a nonmonotonic relationship was observed between vegetable consumption during the first trimester and BWGA (Table 3). None of the categories significantly differed with respect to the highest quintile, but there were differences with the 4th. Newborns of mothers in the first and 2nd quintiles of vegetable consumption weighed 118.3 ± 47.2 g (P = 0.01) and 133.2 ± 45.8 g (P < 0.01), respectively, less than newborns of mothers in the 4th quintile. Fruit consumption had no clear pattern and was only marginally significant (P = 0.08). For the third trimester we found a similar association, with only the newborns of mothers in the first quintile of vegetable consumption weighing 122.2 ± 47.1 g (P = 0.10) less than newborns of mothers in the 4th quintile. Additionally, we explored the association using fruit and vegetable variables adjusted for energy intake (data not shown). Newborns of mothers in the first (148.2 ± 46.6 g) and 2nd (132.5 ± 45.1 g) quintiles of vegetable consumption weighed less (P < 0.01) than newborns of mothers in the 4th quintile. Concerning BLGA, we found a similar pattern to that found for weight, with the first and 2nd quintiles of vegetable intake differing from the 4th quintile, although the difference was only marginally significant (LRT P = 0.05 for both trimesters) (Table 3).

	Discussion

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
In this cohort study of pregnant women in Spain, lower intake of vegetables was associated with an increased risk of having an SGA (weight and length) baby. This risk increase occurred mainly in vegetable intake during the first trimester for weight and during the third trimester for length. Moreover, lower intake of vegetables was associated with decreased BWGA and BLGA. Fruit intake was not associated with either risk of SGA or with BWGA and BLGA.

Fruit and vegetable consumption was previously found to be positively associated with birth weight in 2 cohorts of pregnant women, one from India and another from Denmark (12,13). The 2 studies showed a small, but consistent and significant, increment in birth weight of 6 g per category increment in consumption of green leafy vegetables, after adjustment for covariates, in the Danish study for consumption in quintiles and of 19 g for 3 categories of consumption in the Indian study. The association for fruit was stronger in the Danish study, with a significant increase in birth weight of 10.7 g per quintile. However, in our study we found no association with fruit intake, but an association of vegetable intake with BWGA and BLGA. There was a 63-g difference in birth weight and 0.37 cm in birth length in women in the 4th quintile with respect to the 2 lowest quintiles of consumption. Birth length was only reported in the Indian study, which did not find a significant effect (12). We cannot compare our results with the above mentioned studies, with respect to the risk of having a baby SGA, as they did not report the effects on SGA outcomes. Taken together, our findings suggest that low vegetable consumption may affect the lower tail of the birth weight and length distribution rather than the whole distribution, although we also observed some effect on the whole distribution. Although we could not analyze our data by specific food groups, green leafy vegetables (lettuce or endive, spinach, artichokes) represented almost one-third (27.6%) of the total vegetable consumption in our study population, whereas cruciferous vegetables (cauliflower or broccoli) represented 3.6% and other kinds of vegetables represented 68.6%.

An association between intake of folate, as well as of antioxidants, supplied by fruit and vegetables, and birth outcomes has been reported. In a cohort of pregnant women in Boston (11), no relationship was found between folate or vitamin C intake and birth size, whereas a study in the UK (10) found an increase in birth weight, with a 100-g difference between the lowest and highest tertiles of vitamin C intake, although this difference was reduced after adjustment for other covariates and was considered negligible by the authors. Additionally, some studies have investigated the association between micronutrient status and birth size. For example, a study in Korea reported an increase in birth weight and length with increasing serum concentrations of vitamin C (26). Nevertheless, 2 other studies did not find a significant effect when investigating circulating concentrations of folate or carotenoids (27,28). The apparent lack of association between intake or circulating concentrations of folate or antioxidants and birth size in some studies could be explained by the fact that other unmeasured bioconstituents present in fruit and vegetables could be responsible for their potential benefit. This has been suggested by some studies using fruit and vegetable intake as well as circulating concentrations, which found a benefit of fruit or vegetable intake that persisted even after adjustment for some related biomarkers (12,29).

Like any observational study, this study has limitations as well as strengths. The low participation rate, 54%, may make our results difficult to generalize. In addition, participation bias may not be ruled out if the decision to participate is correlated with maternal conditions that in turn are associated with the risk factor and the outcome under study. We compared participants and nonparticipants regarding sociodemographic characteristics and no significant differences were found except for working status, with a higher proportion of working women among participants (30). Because this variable was not related to either fruit and vegetable consumption or to the birth outcomes under study, it is unlikely that this selection bias could have exerted a significant impact on our results.

It is also possible that fruit and vegetable consumption was related to a healthier lifestyle. In our study, few factors were related to vegetable consumption; younger mothers were more likely to consume fewer vegetables and mothers living in rural areas were more likely to consume more vegetables. Moreover, our region is a horticultural area and fruit and vegetables are widely available and consumed, although we can not completely rule out confounding by unmeasured factors. To address potential problems arising from the dietary intake assessment, we used a FFQ, which is particularly appropriate in studies with a large sample size to assess long term food and nutrient intake. However, it is possible for some type of misclassification to exist.

Our study has many strengths. As a result of the nature of the study design, data were prospectively and accurately collected by trained interviewers, which we consider a positive aspect. Information on all the identified and potential confounding factors was gathered and used in the analysis. We also estimated dietary intake at 2 points during pregnancy, covering the period up to the third trimester. There were few participants lost to follow-up (4%) from inclusion of mothers to delivery, assuring the internal validity of the study. Moreover, the effects persisted after adjustment for the important confounding factors and other important determinants of birth size.

According to our findings, a nonnegligible proportion of women in our study population did not achieve the minimum daily recommended intake of vegetable, 200 g/d (31), and this was associated with less favorable birth outcomes in our study. It would be desirable, from a public health point of view, to reinforce preconceptional as well as prenatal nutritional counseling, in the context of healthier habits, to encourage pregnant women to eat adequate daily amounts of vegetables (apart from potatoes) in accordance with current recommendations.

In conclusion, our study adds insight to the limited data on the association between fruit and vegetable intake and fetal growth. Higher intake of vegetables during pregnancy was associated with higher birth weight and length as well as with a decreased risk of having an SGA (weight or length) baby.

	FOOTNOTES

 
¹ Supported by the Instituto de Salud Carlos III (Red INMA G03/176), Ministerio Sanidad y Consumo (FIS 03/1615, FIS 04/1112, FIS 04/1509, FIS 05/1052, FIS 05/1133, FIS 06/1213, FIS 07/0314), Ministerio Educación y Ciencia (SAF2002-03508).

² Author disclosures: R. Ramón, F. Ballester, C. Iñiguez, M. Rebagliato, M. Murcia, A. Esplugues, A. Marco, M. García de la Hera, and J. Vioque, no conflicts of interest.

⁷ Abbreviations used: BWGA, birth weight adjusted for gestational age and sex; BLGA, birth length adjusted for gestational age and sex; INMA, Infancia y Medio Ambiente; LMP, last menstrual period; LRT, likelihood ratio test; OR, odds ratio; SGA, small for gestational age.

Manuscript received 7 July 2008. Initial review completed 16 August 2008. Revision accepted 21 December 2008.

	LITERATURE CITED

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 

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