Association of Fish and Fish Liver Oil Intake in Pregnancy with Infant Size at Birth among Women of Normal Weight before Pregnancy in a Fishing Community
Inga Thorsdottir1 ,
Bryndis E. Birgisdottir2,
Sveinbjorg Halldorsdottir1 and
Reynir T. Geirsson2
1 Unit for Nutrition Research, Landspitali University Hospital and Department of Food Science, University of Iceland, Reykjavik, Iceland.
2 Department of Obstetrics and Gynecology, Landspitali University Hospital, University of Iceland, Reykjavik, Iceland.
Received for publication August 19, 2003; accepted for publication March 10, 2004.
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ABSTRACT
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This 1998 study investigated the association between intake of fish and fish oil during pregnancy and full-term infants size at birth in an Icelandic fishing community. Healthy women aged 2040 years of normal weight before pregnancy (body mass index: 19.525.5 kg/m2) and at 3843 weeks of gestation were selected randomly. Information on infant size at birth was collected from maternity records. Intake of fish and fish oil in pregnancy was ascertained (n = 491, 80.1%) by using a validated, focused, food frequency questionnaire. Infants of women in the lowest quartile of fish consumption weighed less (p = 0.036), were shorter (p < 0.001), and had a smaller head circumference (p < 0.001) at birth than those of women consuming higher amounts of fish. Infants of women in the highest quartile of fish oil intake (
1 tablespoon (11 ml)/day), consuming threefold the recommended dietary allowance of vitamin A and twofold that of vitamin D, were shorter (p = 0.036) and had a smaller head circumference (p = 0.003) than those of women consuming less. Infant size at birth increased with fish consumption, especially for women in the lower quartiles of consumption. Smaller birth size was linked to the highest levels of fish oil intake. Constituents of fish and fish oil might affect birth size differently depending on the amount consumed.
birth weight; body constitution; dietary supplements; fish oils; fishes; infant; nutrition; pregnancy
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INTRODUCTION
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In both epidemiologic and intervention studies, intake of fish as well as fish liver oil supplements in pregnancy has been positively related to infants birth size (13). It is possible that higher mean infant birth weight in Iceland than in the other genetically related Nordic countries might be related to higher fish consumption (46) and to the large percentage of the population that takes fish liver oil as a daily supplement. The well-established association between smaller size at birth and adult metabolic disturbances such as glucose intolerance, hypertension, and coronary artery disease (710) gives this hypothesis an important dimension. This association may be especially relevant because the prevalence of type 2 diabetes, elevated systolic blood pressure, and coronary heart disease is lower in Iceland than in the genetically related population of neighboring countries (1114). However, in contrast to earlier studies, recent studies have found a high intake of marine fats to be related to lower birth weight and shorter length in the Faroe Islands, another fishing community where birth weight is high (15). Therefore, more knowledge is needed from such communities about the association between consumption of fish products in pregnancy and birth size. Furthermore, fish constituents, that is, fatty acids, have been found to be involved in brain development (16), emphasizing the importance of including head circumference in the analysis, an aspect of birth size not known to have been studied before in a community of high fish intake.
By focusing on women of normal weight before pregnancy, the effect of confounding by maternal body composition is minimized. Information on weight gain in pregnancy related to infant size at birth in the same cohort of normal-weight women was available (17, 18). The aim of this study was to investigate the association between intake of fish and fish liver oil in pregnancy among women of normal weight before pregnancy and their infants size at birth (birth weight, birth length, ponderal index, and head circumference) in a fishing community of high average birth weight.
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MATERIALS AND METHODS
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Women of normal weight before pregnancy (n = 615) were randomly selected by computer from among those who, according to birth records, fulfilled the 1-year inclusion criteria (1998). The women in our study were healthy before pregnancy and did not have a history of hypertension, diabetes, cardiovascular disease, or thyroid problems. They were aged 2040 years, were of approximately normal weight before pregnancy (body mass index: 19.525.5 kg/m2), and delivered singleton infants after a 38- to 43-week gestation (customary definition of "term" at University Hospital in Reykjavik, Iceland) based on routine fetal biometry at an ultrasound examination at 1820 weeks (19). All of the women received early and regular antenatal care, as described earlier (17).
A validated, focused, food frequency questionnaire was sent to the women who agreed to have information collected from their maternity records after the birth of their infant (n = 614, 99 percent of those asked) (17); the rate of response was 80.1 percent (n = 491). This number corresponded to 11.8 percent of all births in the country during the study year. The sample size was calculated to provide a power of at least 90 percent for a p value of <0.05 to detect a change of 0.1 kg in birth weight, 0.3 cm in birth length, and 0.2 cm in head circumference.
From maternity records at the Department of Obstetrics and Gynecology of the University of Iceland, information was collected on prepregnancy, pregnancy, and delivery factorssuch as maternal age, height, marital status, smoking, parity, prepregnant weight, and gestational weight gainas well as on birth outcome. Birth weight and length, head circumference, and the infants condition at birth were recorded. The infant was defined as healthy if no diagnosis of congenital anomaly or disease, including asphyxia or convulsions, was recorded at birth.
The study was approved by the Ethical Committee (institutional review board) at Landspitali University Hospital and by the Icelandic Data Protection Commission.
The food frequency questionnaire asked about frequency of fish intake as a main meal and as part of other meals during pregnancy, the type of fish consumed, and the amount given in portions or pieces. Regarding fish liver oil supplements, the questions were about frequency and amount of intake (capsules, teaspoon or tablespoon) and whether the level of consumption was similar throughout the pregnancy (table 1). Fifteen nursing students validated the food frequency questionnaire by registering their food intake for 14 days (3 days of weighing the items and 11 days of measuring the amounts consumed by using common household objects such as glasses, dishes, cups, and spoons). No difference was found between the two methods regarding frequency or amount of fish liver oil intake. In addition, there was no difference in the frequency of fish consumption (i.e., how often it was eaten per week), but the questionnaire overestimated the amount eaten at each fish meal by 15 percent (p = 0.003) (20), which is well known in the literature (21). The amount of fish or omega-3 fatty acids calculated from fish and fish liver oil intake was categorized in quartiles for the analysis.
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TABLE 1. Main questions in the self-administered food frequency questionnaire completed by pregnant women, Reykjavik, Iceland
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In this paper, the data are described as means and standard deviations as well as percentages. Variables with a skewed distribution were logarithmically transformed. A Wilcoxon signed-rank test for two related samples was used to validate the food frequency questionnaire (n = 15). Analysis of variance was used for trend analysis, and post hoc tests were performed by using least-significant-difference analysis of variance when comparing means between more than two groups. Multiple regression analysis was used to determine the relative importance of relevant predictors with regard to the dependent variables such as birth size. Possible confounding factors were identified from earlier studies (1, 17). These factors were prepregnant weight, weight gain in pregnancy, maternal height, age, parity, smoking, marital status, pregnancy complications, infants gender, and gestational length. When fish was analyzed as an independent value, adjustments were made for fish liver oil intake and vice versa; no interaction was found between the two variables in the models (p > 0.05). The SPSS software program, version 11 (SPSS, Inc., Chicago, Illinois), was used for statistical analysis, and a level of p < 0.05 was considered significant.
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RESULTS
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Maternal and neonatal characteristics of the women (table 2) showed that 60 percent were parous, 8 percent were single, and 16 percent smoked during pregnancy. The characteristics of the women responding to the questionnaire (80.1 percent) and their infants were very similar to those not responding (p > 0.05). Only 1 percent of the women never consumed any fish. Fish liver oil was used as a supplement by 44.8 percent (n = 218) of the women during pregnancy and by 38.7 percent throughout the whole pregnancy. Table 3 shows the amount of fish and fish liver oil consumed and the calculated amount of omega-3 fatty acids, docosahexaenoic acid, eicosapentaenoic acid, vitamin A, and vitamin D obtained from these sources.
Frequency of fish consumption was positively associated with infant birth length (p = 0.007) and head circumference (p = 0.005) (table 4), after adjustment for weight gain in pregnancy, maternal height, parity, smoking, infants gender, gestational length, and intake of fish liver oil. There was no linear association with birth weight (p = 0.098) or ponderal index (p = 0.340). Infants of women in the lowest quartile of fish consumption (020 g/day) weighed less (p = 0.036), were shorter (p = 0.003), and had a smaller head circumference (p < 0.001) at birth than those of women eating more fish per day. Frequency or amount of fish consumption was associated with neither gestational length (p = 0.150) nor weight gain in pregnancy (p = 0.650). Prepregnant weight, mothers age, marital status, and pregnancy complications were not found to affect the relation tested.
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TABLE 4. Mean birth size of infants born to women according to monthly frequency of consumption of fish as a main meal, both before and after adjustment, Reykjavik, Iceland, 1998
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There was no significant difference in gestational length between those who took fish liver oil supplements and those who did not (p = 0.180), and no relation was found with weight gain in pregnancy (p = 0.226). Increasing intake of fish liver oil was inversely associated with infants length at birth (p = 0.040) and head circumference (p = 0.028), after adjustment for weight gain in pregnancy, maternal height, parity, smoking, infants gender, gestational length, and fish consumption. The same results were found for total omega-3 consumption calculated from fish, fish liver oil, and other fish supplements. No relation was seen with birth weight or ponderal index (p > 0.05). Mothers age, marital status, and pregnancy complications were not found to be relevant in the multiple regression model. At birth, the children of women in the highest quartile of fish liver oil supplementation (
1 tablespoon (11 ml)/day) were shorter (p = 0.036) (table 5) and had a smaller head circumference (p = 0.003) (table 5) than those in the group of women with the second lowest intake. Because fish oil supplements in Iceland include vitamins A and D in addition to omega-3 fatty acids, these women had an intake corresponding to three times the recommended dietary allowance of vitamin A in pregnancy and two times that of vitamin D from fish liver oil only, not including vitamins A and D in the diet. No difference in gestational length, birth weight, or ponderal index was found between quartiles of fish liver oil intake (p > 0.05). Of the 16 women whose infants were not defined as healthy at birth, 14 consumed fish liver oil in pregnancy (p < 0.001). High intake of fish liver oil (
1 tablespoon) was more common among those whose child was not diagnosed as healthy at birth (36.4 percent) than among those who delivered a healthy child (19.4 percent) (p = 0.030).
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TABLE 5. Mean birth size of infants born to women according to fish liver oil intake group, both before and after adjustment, Reykjavik, Iceland, 1998
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DISCUSSION
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In a fishing community of high average birth weight, frequency of fish consumption was found to be positively related to both length and head circumference at birth. Infants of women in the lowest quartile of fish consumption were smaller at birth than those of women consuming higher amounts, a finding in accordance with earlier studies (1, 3). However, length was shorter and head circumference at birth smaller in the group of women consuming the highest amount of fish liver oil in pregnancy. The relation between high intake of marine fat in pregnancy and infants head circumference at birth in a fishing community appears not to have been reported before, but recent studies have shown a relation between moderate long-chain omega-3 fatty acid supplementation and intelligence quota at age 4 years (16). In this population whose fish consumption is relatively high, the relation between natural intake of fish, and especially fish liver oil, could be investigated at intake levels similar to or higher than those used in previously described intervention studies of pregnant women (22, 23).
Olsen and Secher (1) found that length of the newborn increased with the mothers frequency of consumption of seafood dinner meals in pregnancy, but only up to about three meals per week or, in another Olsen et al. study (3), 15 g per day. This result is in accordance with ours; after consumption of about 20 g of fish per day, that is, the lowest quartile, no change in birth size was seen with a higher intake. The relation was independent of gestational length in this fishing community cohort of full-term infants, but fish and fish liver oil intake has been found to be related to gestational length in cohorts including preterm infants in a community with low levels of fish and fish liver oil intake (24, 25). It is possible that a large majority of the women in this study were already consuming the minimum amount of fish or fish products necessary to obtain the beneficial effect on gestational length and therefore this relation was not found.
The increase in birth size with fish consumption might be due to a higher intake of long-chain omega-3 fatty acids (1) but might also be attributable to the eventual higher protein consumption or even to protein composition (2). Recent studies suggest earlier unknown variability and bioactivity of fish proteins, which might be of importance (2, 26, 27) and would be very interesting to study. Because no relation was found between fish consumption and weight gain in pregnancy, the higher birth weight of infants born to fish-consuming mothers seems unlikely to be due to a higher energy intake by fish consumers. Although not significant, there was a small decrease in size at birth at the highest fish consumption levels, a trend also found in other studies in fishing communities (15).
Earlier studies showed a positive relation between fish liver oil supplementation and size at birth (1). The inverse relation found in our study is explained by the clearly smaller length and head circumference of infants at birth of those women consuming very high amounts of fish liver oil. Findings from the Faroe Islands, another fishing community of high average birth weight, showed a lower birth weight and shorter length at the highest intake levels of marine fats, and this finding was independent of gestational length (15). To our knowledge, this study shows for the first time smaller head circumferences at high levels of fish liver oil supplementation. This finding might indicate a physiologic effect, that is, that supplementation with fish liver oil has a positive effect on birth size up to a certain point for nations with a low intake (1) but might have a negative effect on birth size at very high intake levels, as also indicated for consumers of high amounts of fish. The smaller percentage of infants defined as healthy at birth among women consuming high amounts of fish liver oil needs further study but adds to the negative information about smaller infant size at birth in the same group of women. The results of this study are important in the context of the relation seen world over between size at birth and adult diseases (10), possibly due to adverse environmental influences in utero, for example, lack of overexposure to certain nutrients (28, 29).
Fish liver oil has many constituents, among them omega-3 fatty acids, which, at high intake levels, animal studies have found to be related to decreased intrauterine growth; however, this finding is disputed because the energy intake of consumers of high levels of these acids was also lower (30). More interesting is that the brand of fish liver oil in use in Iceland also contains vitamins A and D. When the recommended amount of fish liver oil supplementation is exceeded, the dietary reference intakes of vitamins A and D can be greatly exceeded, depending on the composition of the various products on the market in different countries. In this study, more than three times the dietary reference intake of vitamin A came from the fish liver oil (not including vitamin A in the diet) for the group with the highest intake, which is higher than a World Health Organization expert consultation considers safe during pregnancy (31). For example, low intake levels of vitamin D have been related to intrauterine growth retardation (32, 33), which might explain the larger birth size found in some studies where supplementation with fish liver oil occurs, whereas animal studies have related toxic levels of vitamin D to smaller birth size (34). Possible contaminants, such as polychlorinated biphenyls (PCBs) and mercury, also present in fish liver, should be at very low levels in commercial fish liver oil products but can be found in different amounts in different fish species, depending on where they are caught. Grandjean et al. (15) noted that lower birth weight and shorter length linked to a high intake of marine fats in a fishing community were not due to increased exposure to contaminants in seafood. However, such a relation has been found in other studies (35).
In our study, most of the women consuming fish liver oil in pregnancy had been taking supplements before pregnancy; in the intervention studies, use of fish liver oil supplements by women whose intake was habitually low commenced during pregnancy (22, 23), which might partly explain the results. In the same group of women, earlier weight gain in pregnancy has been positively associated with infant size at birth (17).
In Iceland, official recommendations on fish consumption in pregnancy have not existed, apart from fish being considered as contributing to a healthy diet, and modest intake of fish liver oil is recommended for the population as a whole. Official recommendations therefore are not likely to have affected the womens choice of food and supplements in pregnancy, although this possibility can of course not be excluded. This observational study in a fishing community with a habitually high frequency of fish liver oil intake, including women whose intake levels were very high, implies that caution is necessary when freely recommending fish liver oil supplements in pregnancy. Fish consumption should be promoted during pregnancy with the warning that some fishing areas are contaminated.
In an Icelandic fishing community, size at birth increased with consumption of fish, especially for the first quartile of fish consumption. Smaller birth size, in terms of both length and head circumference, was found at the highest levels of fish liver oil intake. The results indicate that constituents of fish and fish liver oil affect birth size differently, depending on the amount consumed, and that moderate consumption should be recommended.
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NOTES
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Correspondence to Dr. Inga Thorsdottir, Unit for Nutrition Research, Landspitali University Hospital, Eiríksgata 29, 101 Reykjavik, Iceland (e-mail: ingathor{at}landspitali.is). 
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