Food patterns and dietary quality associated with organic food consumption during pregnancy; data from a large cohort of pregnant women in Norway

The essential importance of dietary quality during pregnancy for the health of mother and child is continuously becoming clearer, and there is growing evidence that maternal diet may influence longer-term health of their children even within relatively well-nourished populations [1–3].

Dietary composition, the kinds of foods that are eaten and their relative amounts, is together with the nutritional quality of food decisive for the impact of the diet on health. Organic production methods are generally claimed to enhance food quality, and research indicating superior quality of organically produced food include findings of higher levels of vitamins, antioxidants [4, 5], poly-unsaturated fatty acids [6], and lower levels of heavy metals [7], mycotoxins [8] and pesticide residues [9, 10] in a range of crops and/or milk. This matter is far from settled, however, and Dangour et al. [11] suggest, based on a review, that there is not sufficient evidence to draw conclusions about major differences in nutritional quality between organically and conventionally produced food.

In studies from Great Britain, Denmark and Norway, Denver et al. [12], Holt [13] and Torjusen et al. [14] have found associations between the choice of organically produced food and dietary patterns high in fruit and vegetables and low in meat compared to intake levels among consumers who did not buy organic food. It is known from a number of studies that health is a main motivation for choosing organic foods, together with ethical and environmental considerations [15, 16]. Since there is a considerable overlap between dietary recommendations aiming for good health and those aiming for environmental sustainability [17], it is possible to theorize that the choice of organic food for both of these reasons may be accompanied by dietary patterns more in line with health recommendations.

Variation in dietary patterns has been described among pregnant women in several populations, including Norway [18–20]. However, there is little knowledge about the diets of women who choose organically grown food during pregnancy. Given the possibility that the choice of organic food may be related to dietary characteristics of relevance to health, and the particular importance of health during pregnancy, it is important to gain more knowledge about this issue. The Norwegian Mother and Child Cohort Study (MoBa), which is a nation-wide pregnancy cohort [21], includes questions about the frequency of organic food consumption, and thus provides an opportunity to explore possible associations between consumption of organically produced food and dietary composition. We have previously reported socio-economic and lifestyle characteristics associated with frequent consumption of organic food among the MoBa participants. The socioeconomic characteristics of pregnant women with frequent organic consumption did not unambiguously follow those typically associated with better health, such as higher education and income [22]. We also plan to investigate potential diet-health relationships related to consumption of organic food.

The aim of the present study was to examine associations between frequent consumption of organically produced food and the overall dietary patterns, food intake and nutrient density of pregnant women in MoBa. In particular, we wanted to investigate whether there were significant differences in dietary patterns between women who frequently ate organic food during pregnancy and those who seldom or never ate organic food. Furthermore, we wanted to investigate whether there were significant differences between consumption of organic food of different food categories (milk/dairy, bread/cereal, eggs, vegetables, fruit and meat) and diet in general.

Principal component analyses uncovered relatively large variation in reported dietary behavior among the 63808 pregnant women in this study. The first principal component (PC1), accounting for 12% of the variation in food intake among the women (Figure 1), was characterized by high positive loadings for vegetables, fruit and berries, cooking oil, olive oil, whole grain products and negative loadings for meat, including processed meat, white bread, salty snacks, Pommes frites and cakes and sweets. This principal component was denoted a 'health and sustainability component’. The second principal component (PC2), accounting for 7% of the variation in food intake (Figure 1), was characterized by high positive loadings for pasta and rice, poultry, olive oil, cooking oil, and vegetables and negative loadings for yoghurt, potatoes and fruit. This component did not add significantly to the illumination of dietary variation relevant for health, but rather displayed variation in culinary preferences. A cross-validation based on three segments [26] indicates that more than two components in principle could be assessed as significant. There is, however, a clear indication from the scree plot (i.e explained variance plot, in particular for cross-validation) that the first component is clearly dominating with only relatively minor contributions given by the rest of the components. The third and subsequent principal components were not considered because they were not readily interpretable and added less to explained variation in food intake.

These findings were corroborated in the analyses which showed increases in daily intake of food groups characterizing the components, e.g. vegetables (+29 g/d), fruit and berries (+44 g/d), whole grain products (+9.4 g/d), pasta and rice (+4.5 g/d), and decreases in intake of meat (-24 g/d), processed meat (-7.2 g/d), white bread (-15 g/d) and cakes and sweets (-7.7 g/d) among women with frequent consumption of organic food (Table 3). In addition to a higher total vegetable intake, women with frequent organic food consumption ate a larger proportion of raw vegetables (+9 g/day). Regarding beverages, frequent organic consumption was associated with less artificially sweetened soft drinks (-43 g/10 MJ), (but not sugar sweetened soft drinks), less low fat and skimmed milk (-37 g/10 MJ), and more tea (+35 g/10 MJ).

We observed some variations in dietary patterns associated with consumption of the six different groups of organically produced foods (Table 3). The increase in vegetable consumption was particularly high for high consumption of organic vegetables, and the highest increase in consumption of fruit and berries was found among participants with high consumption of organic fruit and berries. High consumption of organic meat represented an exception from the overall associations between frequent organic consumption and dietary patterns: no increase in vegetable consumption, only a small increase in fruit and berries, no decrease in intake of white bread and highly processed breakfast cereals, and only a small reduction in meat intake. Consumption of organic meat was also associated with consumption of more sugar-sweetened soft drinks, and no difference in intake of artificially sweetened soft drinks, contrary to organic consumption of the other five food groups.

A gradual increase in vegetable consumption and a corresponding decrease in meat consumption were evident across increasing frequencies of reported organic consumption (Figure 2). The graphs depict a significant difference in consumption of both meat and vegetables already at the lowest frequency of organic consumption, and that these differences become more pronounced with increasing consumption of organically produced food. Even among women with high scores on PC1 (e.g. high vegetable consumption and low meat consumption), frequent consumption of organic food was associated with higher vegetable consumption and reduced meat consumption compared with women within the same pattern score but with low organic consumption (data not shown).

The results show that rather than a mere ‘substitution’ of conventionally produced foods with organically produced foods of similar types (substituting conventional minced meat with organic minced meat, for example), we see qualitative differences in dietary composition. These qualitative differences include the relative amounts of main food groups (such as less meat and more vegetables), as well as emphasis on different types of products (if meat: rather lamb than sausages,) and food preparation and degree of processing (more vegetables eaten raw, more whole foods rather than highly processed) (see Table 3, Figure 1 and Additional file 3: Figure S1).

Frequent organic consumption and high consumption of all organic food groups were associated with higher energy intake (Table 1). The same was found for the relative contribution of energy from protein. However, the differences in energy contributed by the other macronutrients were small. Furthermore, higher intakes of vegetables, wholegrain products, fruit and berries and lower intakes of processed foods among the frequent organic consumers were reflected in higher relative (energy adjusted) intakes of beta-carotene, ascorbic acid, folate, fiber and magnesium and lower intakes of sodium (Table 1). There were only marginal differences in intake of zinc, selenium and iron between the groups (results not shown).

The main finding of this study was that frequent consumption of organic food among the pregnant women in the MoBa study was strongly associated with higher scores on the ‘health and sustainability component’ (PC1), i.e. a diet characterized by more vegetables, fruit and berries, and whole grain cereal products and less meat, including processed meat, white bread, refined cereal products, cakes and sweets, compared with participants with no or low consumption of organic food. Diets of the pregnant women with frequent organic consumption, consequently, were more in line with dietary recommendations for health as well as ecological sustainability.

In the multivariate part of the present study we have considered data based on first adjusting for amount of food eaten in order to highlight pattern rather than amount. We also decided to exclude beverages when extracting underlying dietary components (patterns) since they had strong dominance on the results. Thirdly we used standardization in order to give all the foods equal opportunity to contribute meaning which means that we consider relative differences in each of the foods rather than the dominating effect of those with the largest variance. This analysis revealed clear differences between ‘healthy’ and ‘unhealthy’ diets represented in particular by the score along the first principal component. In other studies of dietary patterns, contrasting patterns are often found, the first two typically being ‘prudent’ and ‘western’ (or denoted with similar names) [18, 27–29]. In the present study, however, both ‘healthy’ and ‘unhealthy’ diets are covered by the first principal component, represented by high and low scores, respectively. This dual dimension within the first component was also seen in a large cohort of pregnant women in Southampton [30, 31]. The first principal component extracted in that study was characterized by high intakes of healthy food items vs. unhealthy food items.

In the present study, two types of food issues were brought together: How food is produced and what kinds of foods that are eaten. The findings confirm that in the dietary practices of the pregnant women in this study, there was an association between these two food dimensions. We have no means of knowing the order in which choices were made and practices established: Did the choice of buying organically produced food form the choice of diet, or did more people who preferred certain types of diets choose organically produced foods – or did reflection about both these aspects of food mutually influence each other? Regardless of how these practices have developed, the significant differences in dietary characteristics are of relevance with regard to their ability to contribute to good health and ecological sustainability. Dietary recommendations aiming at both these goals are to a large extent overlapping. Central to ecological sustainability is eating lower in the biological food chain (i.e. more plant foods and less meat), because it maximizes the amount of high quality food for human nutrition relative to the ecological costs of production, and this also fits well with health advice.

We have previously reported a large difference in prevalence of vegetarians (+23 percentage points) among the pregnant women in MoBa who frequently ate organic food compared to those who did not [22]. Since the total number of vegetarians was very low, however, (0.2%, ibid) the practical significance of the change in dietary pattern expressed as a shift of the whole group of frequent organic consumers from lower to higher scores on the ‘health and sustainability component’ (PC1) is by far much larger. An implication of this was that on average, the frequent organic consumers in the MoBa-study had a reported intake of over half a kilo more vegetables, fruit and berries weekly than those with low organic consumption, and they reached the Norwegian recommendations of ‘5 a day’ (500 g vegetables, fruit and berries a day), while those with no or little organic food in their diets were 65 g short of doing so.

In addition to a higher total consumption of vegetables, women with frequent organic consumption also ate a larger proportion of these vegetables raw. Higher intakes of ‘whole foods’ such as raw vegetables, fruit and berries, nuts, wholegrain bread and cereal products among the frequent consumers of organic food in the present study are in line with preferences for less processed and refined foods as reported by both Holt [32] and Torjusen [33], as well as consumers’ associations of organic food with characteristics such as ‘natural’ and ‘home made’ [16, 34]. Similarly, lower consumption of refined and processed foods such as processed meat, highly refined cereal products, potato chips (‘salty snacks’) and Pommes frites further confirms such trends. Characteristic in this respect is also the negative correlation between tomato ketchup and fresh tomatoes, as representatives of diets with ‘fast food’ or processed food vs. diets based on fresh produce and whole foods (see details in Additional file 3: Figure S1).

There was large variation in use of different types of fat in the diet (Figure 1), and the association between frequent consumption of organic food and more use of olive oil and cooking oil, which is in line with previous findings [33], may be related to a larger emphasize on health among those who choose organic food.

The observed negative correlation between processed meat and meat from intensive production systems (such as pork) with negative loadings and meat from extensive production (lamb), with positive loadings on the ‘health and sustainability component’ (Additional file 3: Figure S1), may be interpreted in light of ecological consciousness or a preference for what is perceived as more ‘natural’ or ‘closer to nature’.

In her study of dietary habits among organic consumers in the UK, Holt reported a shift away from a diet focused on meat, potato and bread, towards increased consumption of vegetable foods and in particular, the incorporation of non-traditional plant foods, such as nuts, pulses and grains into the diet, resulting in a greater diversity of protein and staple foods among consumers of organic foods [13]. In the present study, frequent consumers of organic food had slightly lower percentage of energy derived from protein (Table 1), as well as a higher relative proportion of proteins from plant foods rather than animal foods, but still a protein intake well within (and in the upper levels of) dietary recommendations for pregnant women [35]. Higher intakes of foods such as nuts, pulses and legumes and soy products represent alternative sources of proteins in diets with less meat. We also recognize more diversity in ‘staple foods’: higher intake of less traditional grains such as millet, as well as higher intake of pasta and rice (Figure 1 and Table 3).

Our finding of higher average energy intake among frequent organic consumers (about 600 kJ/day more, Table 1) is likely to be related to higher levels of physical activity, as we have previously found that a larger proportion of the frequent organic consumers in the MoBa-study exercised regularly and were normal or low weight compared to those with no or low organic consumption [22]. Their food intake therefore seems to be more in balance with their energy expenditure.

The large sample size including women from both urban and rural regions, representing all age groups and socio-economic groups is a major strength in the present study. The large sample size ensures large variation in dietary composition and use of organically produced food. However, only 38.5% of those who were invited participate in MoBa, which imply that the prevalence of organic consumption may not be representative for all pregnant women in Norway. The potential influence of self-selection in MoBa has been evaluated, and no statistically relative differences in association measures were found between participants and the total population regarding eight exposure-outcome associations [36]. Hence, the selection bias in MoBa is not likely to influence the associations between reported use of organic food and dietary behavior among the frequent organic consumers. The sum index is a relatively crude measure, but in spite of this we observed important associations between overall frequent organic consumption and dietary quality. We also observed differences in food and nutrient intakes between frequent consumers of the various organic food groups. When designing a new FFQ, as was done for the MoBa cohort, there is a trade-off between the number of questions and the burden imposed on respondents. If questionnaires ask in too much detail there is an increased risk of participant drop-out [37, 38]. We do not know how the MoBa FFQ influenced the participation rate, but 93% of the women participating in MoBa did answer the FFQ [21].

Misreporting is a serious error in all dietary assessment methods [39], and it has been shown that foods perceived as ‘unhealthy’ are underreported to a larger degree than foods perceived as ‘healthy’ [40]. The food frequency methods challenges participants with complex cognitive tasks and is particularly difficult to answer early in pregnancy when many women are experiencing nausea and changes in appetite and eating patterns. However, the MoBa FFQ was developed and validated for use in pregnancy [24] and the validation study demonstrated that relative to a dietary reference method and several biological markers, it produces a realistic estimate of the habitual intake and is a valid tool for ranking pregnant women according to high and low intakes of energy, nutrients, and food [41].

We have previously reported that frequent consumption of organic food among pregnant women in the MoBa-study was not solely associated with socio-economic and lifestyle factors that are normally associated with good health [22]. While women who consumed organic food exercised more frequently, a larger proportion of them also consumed alcohol and smoked during pregnancy (although total prevalences were low). Lower household income and lower as well as higher levels of education were associated with frequent organic food consumption. While the consumption of organic food was not typically associated with high socio-economic status and healthy lifestyle factors, the association between frequent organic consumption and diet quality appeared to be clearer: pregnant women who chose organically produced food also ate diets that were more in line with health recommendations. Dietary quality is especially critical in pregnancy and PCA-derived dietary patterns in pregnancy have been associated with various health outcomes in well-nourished populations, including gestational weight gain [42]), preeclampsia [18], foetal growth [43] and post-partum depression [44]. There are, however, few previous studies addressing the combination of organic food consumption and the general dietary patterns and quality among pregnant women.

A methodological implication of the present study is that information about the diet in general needs to be included in future studies of possible health outcomes related to organic food consumption. It will further be advantageous to have specific information about consumption of organic food of different food groups, since high consumption of organic meat was associated with a somewhat different dietary pattern than that of organic vegetables, fruit, cereal products, dairy products and eggs.

Large knowledge gaps remain in our understanding of the consumption of organic food, related food practices and possible implications for health of mother and child. It remains an unsettled question whether there are systematic differences in the absolute content of nutrients and other substances of importance for health in foods that are organically or conventionally produced. The food analyses in the present study are based on the same food tables for both organically and conventionally produced foods, because at present there are no separate data on organically produced foods in the form of systematic food tables. If such differences are present, estimates of nutrient intakes would be imprecise or wrong. There are knowledge gaps in our understanding of how the consumption of organic food may be related to health, both in short and long term. Findings that indicate possible associations between consumption of organic food and health, such as prevalence of allergic diseases among children in families with organic consumption [45, 46], will be addressed in future studies.

The present study showed that pregnant Norwegian women reporting frequent consumption of organically produced food had a dietary pattern and quality more in line with public advice for healthy and sustainable diets. A methodological implication is that the overall diet needs to be included in future studies of potential health outcomes related to consumption of organic food during pregnancy.