The quantity and quality of the maternal diet during pregnancy is of extreme importance, not just for the health of the mother, but also for the health and development of the fetus, and for the outcome of the pregnancy. In fact, the influence of the maternal diet during pregnancy reaches even further in its impact; it may have permanent effects on the health and well-being of the offspring in later life(Reference Barker1). A large body of animal study data have provided evidence that maternal diet is associated with the outcome of the pregnancy, as well as with the offspring’s lifespan and health in adulthood(Reference Waterland and Garza2). Human studies, with data derived mostly from situations of food shortage, have also indicated a link between maternal nutritional status and newborn size, and further between low birth weight and increased risk of adult chronic disease(Reference Prentice, Cole and Foord3). Epidemiological data from well-nourished populations, however, paints a more contradictory picture(Reference Fall4).
A number of maternal factors have been established to influence fetal growth and pregnancy outcomes in well-nourished populations. Apart from cigarette smoking, many of the other factors, such as low pre-pregnancy BMI or low gestational weight gain, are indicators of maternal nutritional status(Reference Kramer5). Both inadequate and excessive intake of certain nutrients have been related to undesired birth outcomes and pregnancy complications(Reference Rothman, Moore and Singer6, Reference Tamura and Picciano7). A further evolving issue is the prevalence of overweight and obesity, which has been linked to health risks for pregnant women and their babies(Reference Henriksen8). Maternal intake of energy-yielding nutrients, vitamins and minerals during pregnancy, especially during certain ‘sensitive periods’, has also been implicated to influence placental weight and the size of the newborn(Reference Haste, Brooke and Anderson9–Reference Moore, Davies and Willson11). The combination of these sensitive periods and seasonal variation in food consumption and nutrient intake could potentially influence birth outcomes. A recent pilot study from New Zealand was able to link the seasonal variations found in the nutrient intakes of pregnant women, with the differences in birth measures across different seasons(Reference Watson and McDonald12). In Finland, although the diet of the average pregnant woman is thought to be fairly healthy, studies have revealed inadequacies in the intake of folate, iron and vitamin D(Reference Arkkola, Uusitalo and Pietikäinen13, Reference Erkkola, Karppinen and Järvinen14). In a Northern country like Finland, with its extreme variation in climate, the availability and price of fresh foods are most likely to exhibit seasonal variation, and hence temporal differences in food consumption are to be expected.
We set out to study the food consumption and nutrient intakes in a large cohort of pregnant Finnish women. First, we examined whether the food consumption and nutrient intake had changed over the study years, within this cohort of women. Particular attention was paid to whether the optional vitamin D fortification of all fluid milk products and fat spreads that started in February 2003 had had any significant impact on the intake levels(15). We then proceeded to look for seasonal variations in the consumption of certain foods and food groups, and in the levels of nutrient intakes. On the basis of our findings, we went on to highlight specific areas of concern, and to raise issues that might warrant discussion on maternal diet during pregnancy.
Subjects and methods
Subjects
The Type 1 Diabetes Prediction and Prevention (DIPP) project is a multi-disciplinary population-based birth cohort of children with increased genetic risk for type 1 diabetes. The present study is designed to predict the development of type 1 diabetes, and to search for means to prevent or delay progression to clinical type 1 diabetes(Reference Kupila, Muona and Simell16). All newborn infants in the areas of three university hospitals were screened from cord blood, for major histocompatibility complex, class II, DQ beta 1 (HLA-DQB1) conferred susceptibility to type 1 diabetes, and families with a risk child were invited to participate in the DIPP study. Ethical approval was obtained from the local ethics committees of the participating university hospitals of Turku, Oulu and Tampere. All families participating in the study signed an informed written consent.
The present study is part of the DIPP Nutrition Study, which is being carried out within the framework of DIPP in the university hospitals of Oulu and Tampere. Mothers from the DIPP Study, whose infants carried increased risk for type 1 diabetes were invited through their delivery hospital, to take part in the Nutrition Study. The focus of the nutrition arm is to examine the effects of maternal nutrition during pregnancy and lactation, and of the child’s diet, on the development of β-cell autoimmunity, type 1 diabetes, asthma, allergic diseases and obesity in the offspring. The present study consists of mothers of at-risk children born between 20 October 1997 and 5 September 2004. Baseline dietary data were available from 4942 mothers, of whom sixty-two had returned dietary data questionnaires with missing consumption frequencies for ten or more food items. These mothers were omitted from the study, thus leaving us with a final sample size of 4880 (68·3 % of those invited to the study; Table 1).
General characteristics of the study population (n 7147)
*Quit smoking during first trimester of pregnancy.
†Dietary data not available, supplement use not known.
Dietary assessment
The maternal diet during pregnancy was assessed using a validated, self-administered 181-item FFQ(Reference Erkkola, Karppinen and Javanainen17). The FFQ was designed to reflect the diet of Finnish women of reproductive age. The participants received the questionnaire after delivery and returned it at their infant’s 3-month visit to the study centre. The information gathered reflected their diet during the 8th month of pregnancy. As this period immediately precedes the time when Finnish mothers start their maternity leave, it is likely to best represent their average diet during pregnancy. The frequency options for the consumption of foods and food groups were ‘not at all’ or ‘number of times per day’ and ‘week’ or ‘month’. The respondents were asked to report the consumption frequencies in natural units (e.g. one orange), common household measures (e.g. one glass of milk) or portions (e.g. one portion of lasagne). Since the effect of the pregnancy diet is likely to be modified by differences in the use of food supplementation, the FFQ included an open section to collect information on any supplementation used during the entire pregnancy(Reference Arkkola, Uusitalo and Pietikäinen13). The FFQ was checked by a trained study doctor or nurse, and where necessary, completed in consultation with the mother. All returned FFQ were also double-checked by a trained nutritionist.
For the present analysis, we split the food consumption data into ingredients using a recipe composition from the Finnish Food Composition Database (FCDB) Fineli(18). Two updated versions of the FCDB were used: the first version for study years 1997–2002 and the second version for years 2003–2004. Recipe compositions were changed from the first version to the second in order to reflect changes in food consumption habits that took place during the study period as new foods and food products entered the market. Between the two versions, the compositional changes affected 57 % of the food items in which either the ingredients in the recipes or proportions of ingredients, or both were changed. The changes in recipes were mainly based on food consumption information of women aged 25–44 years from the national dietary surveys, FINDIET 1997(19) and FINDIET 2002(Reference Männistö, Ovaskainen and Valsta20), respectively. Vitamin D concentrations were systematically changed in milk and fat products due to changes in fortification in 2003(15). An in-house software program of the National Institute for Health and Welfare was used to convert the food consumption and supplement intake data into a daily food diary, and to generate mean daily food, energy and nutrient intakes. Since the mean daily intake of nutrients from supplements was calculated for the whole tenor of pregnancy, seasonality of supplemental nutrient intake was not examined. However, daily nutrient intakes from supplements were included in the seasonality analysis in order to assess the overall nutrient intake levels for the present study population.
Information on sociodemographic characteristics was registered by a structured questionnaire or obtained from the Finnish Birth Registry. Smoking during pregnancy was divided into three categories (smoker, non-smoker and quit smoking during the first trimester). However, since the number of those who quit was very small, they were grouped together with the smokers.
Data analysis
A χ 2 test was used to test for differences in the demographic variables between the women with dietary data, and those without. Mean nutrient intakes were calculated based on the maternal food consumption during the 8th month of pregnancy, which in turn was determined from the child’s birth date. The mean consumption of selected food groups and the intake of nutrients were also calculated according to season (spring, March–May; summer, June–August; autumn, September–November and winter, December–February). ANOVA was used to test for differences in food consumption and nutrient intake between year-groups and seasons. For those variables that were not normally distributed, logarithmic transformation was carried out before the analysis. Variables that showed non-normality even after logarithmic transformation were tested using a non-parametric Kruskal–Wallis test. In addition, pairwise tests were performed using Bonferroni corrections. However, since the Bonferroni correction can be rather stringent, we have reported associations at the conventional level of significance (P < 0·05) while taking into account the results of the Bonferroni correction in interpreting our results. Seasonal effects were also tested so that maternal age, education and the number of earlier deliveries were included as covariates in the model. Statistical analyses were carried out with SAS for Windows statistical software package version 8·2 (SAS Institute Inc., Cary, NC, USA).
Results
Table 1 shows the sociodemographic characteristics of the women who participated in the study, as well as of those who did not provide dietary data. Women who did not provide dietary data (n 2267) differed from those who did (n 4880) in terms of age, education, smoking status during pregnancy, parity and gestational age. Women aged < 25 or ≥ 35 years, women whose education was below high-school level, and women with two or more children were all under-represented among the women who provided FFQ data. Large proportion of women who provided dietary data complemented their diet with dietary supplements (78 %).
When we examined the intakes of energy-yielding nutrients from foods expressed in relation to energy intake by year of pregnancy, we found that the mean proportion of energy derived from fat had decreased over the study period, whereas the mean proportions of protein and carbohydrate from energy intake had increased (Table 2). There was a significant increase in the intake of vitamin D both from food sources and supplements against the year-group 2003–2004. However, after the Bonferroni adjustment, the year-group differences in the intake from supplements were no longer significant.
Mean (sd) daily intakes of energy-yielding nutrients from foods and supplements expressed in relation to energy intake (E%/MJ) by year-groups
Intake of vitamin D is expressed as absolute mean daily intakes (μg) from food sources and supplements together and separately.
*Difference between year-groups tested with non-parametric Kruskal–Wallis test.
Our data showed seasonal fluctuations in the consumption of vegetables, fruits and berries and cereals, and also in the consumption of specific food items such as rice and pasta, sausages, processed meat, ice cream, tea and soft drinks (Table 3). The overall vegetable intake was highest in the summer and lowest during winter. Seasonal differences were also observed within the vegetable subgroups. The consumption of vegetable fruits exhibited significant variation across seasons. The mean daily consumption of fruits and berries was lowest during the summer while berry consumption on its own peaked during summer and autumn. There was significant seasonal fluctuation in the consumption of the imported citrus fruits, with the highest intakes in the winter. Cereal consumption differed significantly between summer and autumn. Sausages, ice cream and soft drinks were most frequently consumed in the summer, with ice cream showing significantly different consumption levels across seasons. The consumption of tea was highest in the autumn and winter.
Mean daily consumption (g) of selected food groups and foods in the diets of pregnant Finnish women by seasonFootnote *
* Seasons are defined as spring, March–May; summer, June–August; autumn, September–November; and winter, December–February.
† Difference between seasons tested with non-parametric Kruskal–Wallis test.
When we examined seasonality in the intake of nutrients, we found variation in the intakes of dietary fibre, total fat and MUFA (Table 4). The proportion of energy from total fat was significantly higher in the summer compared to other seasons. The proportion of energy intake from MUFA was also at its highest during summer. The intake of dietary fibre was at its lowest during summer. The intake of vitamin D showed seasonal differences with significantly lower intakes in the autumn. Folate intake was lowest in the summer and highest in the winter, whereas higher vitamin E intakes were observed during the summer months. There were significant differences in the intake of iron between spring, summer and autumn. Although the intakes of vitamin A and C were also found to exhibit seasonal variation, the results after Bonferroni corrections were no longer significant.
Mean daily nutrient intakes from foods and supplements for pregnant Finnish women by seasonFootnote *
* Seasons are defined as spring, March–May; summer, June–August; autumn, September–November; and winter, December–February.
† Difference between seasons tested with non-parametric Kruskal–Wallis test.
We used the ANOVA to adjust for maternal age, education and parity on our seasonality results. Overall, our results headed towards more significance post adjustment, indicating a true seasonality effect (data not shown). The only exception was the intake of carbohydrate in which, after adjustment, the difference in the intake across seasons was no longer significant (P = 0·077).
Discussion
In the present study, we described the diet of pregnant Finnish women over a period of 7 years, with special attention paid to seasonal fluctuations in food consumption and nutrient intake, and to any significant changes in nutrient intakes over the study period. As far as we are aware, this is the first study in Europe to link the food consumption and nutrient intake of pregnant women to seasonality.
Our findings indicate an overall improvement in the diet of pregnant Finnish women over the study period. These results are mostly in line with the FINDIET 2007 Survey(Reference Paturi, Tapanainen and Reinivuo21), which documented a general improvement in the dietary habits of the adult Finnish population as a whole. We found that over the study period, the mean daily energy derived from fat decreased, while there were increases in the energy derived from protein and carbohydrate, and in the intake of dietary fibre. Our results also illustrate a considerable leap in vitamin D intake from food sources between the 2001–2002 and 2003–2004 year-groups, reflecting the effect of fortification of liquid milk products with vitamin D(15). Seasonal differences in food consumption were accompanied by corresponding variations in the intake of nutrients. Even with the inclusion of intakes from supplementation, the mean intakes of vitamin D and folate fell below the recommended levels throughout the year(22).
The main strength of the present study was the use of a large, population-based cohort. Given that virtually all childbirths in Finland take place in public hospitals, the study sample was likely to be a close representation of the overall population of pregnant Finnish women within the university hospital areas in the present study(Reference Uusitalo, Uusitalo and Ovaskainen23). A further strength of the study was the use of an FFQ that was designed specifically for the DIPP Nutrition Study and found to rank participants reasonably well according to their dietary intakes(Reference Erkkola, Karppinen and Javanainen17).
However, the study is not without its limitations, and these were related mostly to the use of the FFQ method and its potential for information bias. Since the mothers filled in the FFQ retrospectively, the influence of current diet is a possible source of bias(Reference Bunin, Gyllstrom and Brown24). However, when the FFQ used in our study was validated, it was found that FFQ and food records completed 1 month after delivery, agreed well with those completed during the 8th month of pregnancy, indicating that the influence of current diet on our results was likely to be minimal. Another bias may be caused by seasonal reporting which has been shown to afflict the use FFQ(Reference Subar, Frey and Harlan25). We also found that our study sample was biased towards women with higher education and a smaller number of children (Table 1). These respondents are likely to be more health conscious than the non-respondents, which may have had some bearing on our results.
The differences in food consumption between seasons, observed in our study, are most likely a result of cultural habits and seasonal changes in the availability and price levels of fresh food products in Finland. Our observations of seasonal patterns in the consumption of fresh food products are in accordance with the annual purchase reports on vegetable consumption in Finland(26). In the autumn and winter, roots and tubers were popular, whereas leafy vegetables and vegetable fruits formed a larger part of the diet in the spring and summer, and citrus fruits were favoured in the winter. Consumption of staple foods, such as potatoes, was found to be fairly constant over the seasons, as has been reported in earlier studies(Reference Ziegler, Wilcox and Mason27). Although overall fruit and berry consumption was lowest in the summer, the abundant supply of strawberries in the summer leads to their consumption, overshadowing that of other berries, the effect of which can be seen in our study. The long Finnish summer holiday season and the resulting change in dietary behaviour are likely explanations to the increased consumption of sausages (commonly barbequed), ice cream and soft drinks during the summer. The holiday season has been identified as influencing dietary habits and causing small increases in body weight(Reference Hull, Hester and Fields28). Higher consumption of tea in the autumn and winter is a likely reflection of the adjustment to the cold season.
In line with most studies to date, we did not observe significant seasonal differences in daily energy intake(Reference Hackett, Appleton and Rugg-Gunn29–Reference Van Staveren, Deurenberg and Burema31). Neither did we observe significant seasonal fluctuations in the proportion of energy derived from protein, which is in agreement with findings from previous reports(Reference Hackett, Appleton and Rugg-Gunn29, Reference Ma, Olendzki and Li32–Reference Krauchi and Wirz-Justice34). Earlier studies have, however, reported seasonal differences in the intake of fat, with the highest intakes occurring during winter(Reference Shahar, Froom and Harari30, Reference Van Staveren, Deurenberg and Burema31), spring(Reference Watson and McDonald12, Reference Van Staveren, Deurenberg and Burema31) and autumn(Reference Ma, Olendzki and Li32). We observed that the proportion of energy derived from total fat exhibited seasonal changes was highest in the summer, this being the result of the holiday season and the dietary changes mentioned earlier. We further observed that the intake of dietary fibre was lowest in the summer, when consumption of cereals, and the overall consumption of fruits and berries was at its lowest as well. Lower intakes of dietary fibre in the summer have also been reported in previous studies(Reference Watson and McDonald12, Reference Van Staveren, Deurenberg and Burema31).
Our data showed the lowest folate intakes in the summer, with mean intake levels falling below the recommendation during pregnancy throughout the year(22). This confirms earlier findings of low folate intake in a large proportion of pregnant Finnish women(Reference Arkkola, Uusitalo and Pietikäinen13, Reference Erkkola, Karppinen and Järvinen14) despite the recommendations to increase the consumption of folate-rich foods during pregnancy(Reference Hasunen, Kalavainen and Keinonen35). At this time, there are no folate supplementation recommendations for pregnant women in Finland, except in cases of poor dietary habits, certain illnesses or neural tube defects in the family. However, our results indicate a need to look for stronger and more persuasive ways to increase folate intake during pregnancy to ensure adequate intake levels for all pregnant women.
Although we did observe an improvement in the intake levels of vitamin D from food sources over the study years, this cohort’s mean intake in 2003–2004 still did not reach the target recommendation of 10 μg per day (400 IU)(22). Because of the increasing evidence of the importance of vitamin D in the prevention of many chronic diseases(Reference Holick36–Reference Erkkola, Kaila and Nwaru38), there is a clear need to find ways to promote vitamin D supplementation. Past studies have shown that only around 30–40 % of pregnant Finnish women adhere to the vitamin D supplement recommendation(Reference Arkkola, Uusitalo and Pietikäinen13, Reference Erkkola, Karppinen and Järvinen14). Although dietary means alone are likely to be insufficient to tackle the inadequate intakes, a diet comprised of more fish and margarines would be a step towards the right direction. Recent discussions have urged a revision of both vitamin D fortification policies and supplement recommendations(Reference Hollis39, Reference Tylavsky, Cheng and Lyytikäinen40).
In conclusion, our findings indicated positive changes in the diet of pregnant Finnish women over the 7-year study period. We did, however, identify areas needing further improvement; in particular, the type of fat in the diet and the intake levels of folate and vitamin D. To achieve the standards set by the Finnish nutrition recommendations, there is a need to cut down the intake of saturated fat while increasing the intake of PUFA(22). There is also a call for increasing the intake of energy derived from carbohydrate while cutting down the intake of sucrose, which can be achieved by adding more unrefined cereals, vegetables, fruits, berries and potatoes into the diet. High intake of the above-mentioned foods is a step towards an overall healthier diet and will in addition help to reduce the intake of saturated fat and add more dietary fibre in the diet.
Since optimising the nutritional status of pregnant women is extremely beneficial for both the mother and the child, the health-care sector can only gain from paying special attention to maternal nutrition. Nutritional counselling by health-care workers through the child health-care clinics has limited time to reach the larger population of women of reproductive age, and new ways are needed to communicate the importance of pregnancy diet. In this modern age, the Internet offers an efficient way to reach a large part of the target group, especially in Finland where Internet usage is high and discussion groups on some ‘mother & baby’ magazine sites are the most popular in the country.
Acknowledgments
The study was supported by the Academy of Finland (Grants 63672, 79685, 79686, 80846, 201988, 210632, 129492 and 126813), the European Foundation for the Study of Diabetes, the Finnish Diabetes Research Foundation, the Finnish Paediatric Research Foundation, the Juho Vainio Foundation, the Yrjö Jahnsson Foundation, Medical Research Funds of Turku, Oulu and Tampere University Hospitals, the Juvenile Diabetes Research Foundation (Grants 197032, 4-1998-274, 4-1999-731 and 4-2001-435), the Novo Nordisk Foundation and EU Biomed 2 (BMH4-CT98-3314), Doctoral Programmes for Public Health and the Jalmari and Rauha Ahokas Foundation. None of the authors had financial or personal interests in any company or organisation sponsoring the research at the time when the research was carried out. The authors are extremely grateful to all the families who took part in the present study. They would like to acknowledge the dedicated collaboration of the DIPP research nurses, doctors, nutritionists and laboratory staff over the years. Many thanks are also extended to Tommi Korhonen, Suvi Ahonen and Maija Salmenhaara for their help with data management.
