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J. Nutr. First published December 17, 2008; doi:10.3945/jn.108.095745
 Journal of Nutrition, doi:10.3945/jn.108.095745
Vol. 139, No. 2, 298-304, February 2009
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© 2009 American Society for Nutrition

Nutrient Requirements and Optimal Nutrition

Maternal Fish Oil Supplementation during Lactation May Adversely Affect Long-Term Blood Pressure, Energy Intake, and Physical Activity of 7-Year-Old Boys1–3,

Marie Asserhøj4, Sofie Nehammer4, Jeppe Matthiessen5, Kim F. Michaelsen4 and Lotte Lauritzen4,*

4 Department of Human Nutrition, Faculty of Life Sciences, University of Copenhagen, DK-1958 Frederiksberg, Denmark and 5 National Food Institute, Technical University of Denmark, DK-2860 Søborg, Denmark

* To whom correspondence should be addressed. E-mail: ll{at}life.ku.dk.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Subjects and Methods
 Results
 Discussion
 LITERATURE CITED
 
Early nutrition may program obesity and cardiovascular risk later in life, and one of the potential agents is (n-3) long-chain PUFA (LCPUFA). In this study, our objective was to examine whether fish oil (FO) supplementation during lactation affects blood pressure and body composition of children. Danish mothers (n = 122) were randomized to FO [1.5 g/d (n-3) LCPUFA] or olive oil (OO) supplementations during the first 4 mo of lactation. The trial also included a high-fish intake reference group (n = 53). Ninety-eight children were followed-up with blood pressure and anthropometry measurements at 7 y. Diet and physical activity level (PAL) were assessed by 4-d weighed dietary records and ActiReg. The PAL value was 4% lower (P = 0.048) and energy intake (EI) of the boys was 1.1 ± 0.4 MJ/d higher (P = 0.014) in the FO group than in the OO group. Starch intake was 15 ± 6 g/d higher (P = 0.012) in the FO group, but there were no other differences in diet. Body composition did not differ between the randomized groups with or without adjustment for starch intake, EI, and PAL. FO boys had 6 mm Hg higher diastolic and mean arterial blood pressure than OO boys (P < 0.01), but girls did not differ. Within the randomized groups, blood pressure was not correlated with maternal RBC (n-3) LCPUFA after the intervention, but PAL values were (r = –0.277; P = 0.038). We previously found higher BMI at 2.5 y in the FO group, but the difference did not persist. The differences in blood pressure, EI, and PAL, particularly among boys, suggest that early (n-3) LCPUFA intake may have adverse effects, which should be investigated in future studies.


   Introduction
TOP
 ABSTRACT
 Introduction
Subjects and Methods
 Results
 Discussion
 LITERATURE CITED
 
It has been hypothesized that early nutritional influences may determine differences in predisposition to lifestyle diseases, such as obesity and cardiovascular disease. Obesity and hypertension have been shown to track from early infancy and childhood on to adulthood (1,2). Studies in animals have shown that this tracking is in part due to the programming effects of early nutrition (3). (n-3) long-chain PUFA (LCPUFA)6 has been hypothesized to be a programming factor contributing to the beneficial effects of breast-feeding (4,5). A long-term effect of LCPUFA in infant formula has been found on blood pressure in 6-y-old children (6). Furthermore, an (n-3) PUFA-deficient diet during perinatal life has been shown to have a significant programming effect on mean arterial pressure (MAP) in rat offspring (7). In vitro and animal studies have shown that eicosanoids derived from arachidonic acid play a role in adipocyte development and that this effect may be inhibited by docosahexaenoic acid (DHA) and eicosapentaenoic acid from the (n-3) LCPUFA family (8).

An increasing number of infant formulas contain LCPUFA, to mimic the composition of breast milk. The (n-3) LCPUFA concentration in breast milk varies with maternal diet and is especially influenced by the intake of fish or fish oil supplements (9). Early intake of (n-3) LCPUFA has been shown to affect the development of central nervous system functions, such as visual acuity, but the optimal intake is not known (9). A number of maternal fish oil supplementation trials have been performed to examine if variations in breast milk (n-3) LCPUFA can affect functional outcomes in the infants (10–12). None of these studies have investigated the long-term effects on health markers beyond infancy and early childhood.

We performed a randomized trial in which lactating Danish mothers were supplemented with either fish oil (FO) or olive oil (OO) for the first 4 mo of lactation (12). A previous follow-up of the children at 2.5 y of age showed that this may have long-term effects on BMI, which was higher in the FO group (13). The aim of the present 7-y follow-up study was to investigate the effect of maternal (n-3) LCPUFA consumption during lactation on body composition and blood pressure in the now 7-y-old children. Diet and physical activity were also examined primarily to control for the confounding effect of these variables. Furthermore, we performed cognitive assessments in the children, but these results will not be included in the present paper.


   Subjects and Methods
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
Results
 Discussion
 LITERATURE CITED
 
The present 7-y follow-up study was based on a double-blind, randomized, controlled intervention trial (12), including a previous 2.5-y follow-up study (13), approved by the Scientific-Ethical Committees for Copenhagen and Frederiksberg (KF 01–300/98, KF 01–183/01, and KF 11321572). Both parents of each child gave written consent to participate in the 7-y follow-up after the study had been explained to at least 1 parent orally as well as in writing.

    Participants. Pregnant Danish women were selected for the intervention trial among those recruited for the Danish National Birth Cohort (14). Women in mo 8 of pregnancy living in the greater Copenhagen area and having a fish intake below the population median [equivalent to an intake of <0.40 g/d of (n-3) LCPUFA] were asked to participate in the randomized trial. Women with a fish intake in the highest quartile [>0.82 g/d of (n-3) LCPUFA] were also asked to participate in the trial as a high-fish–intake reference group (HF group). Briefly, all the women had to be healthy and to give birth to normal-weight term singleton babies [for further details, see (12)].

    The intervention. The trial was carried out as a double-blind trial throughout the intervention period (12). Those examining the children at both the 2.5-y and 7-y follow-ups were not aware of the group allocation, but the participants were informed about their group at the age of 1–2 y. The design of the trial is presented in Figure 1. After delivery, the women with the low fish intake were randomly allocated to 2 supplementation groups: an experimental group receiving the FO supplement (containing 0.6 g/d eicosapentaenoic acid and 0.8 g/d DHA) or an OO control group as described in (12). The mean self-reported compliance throughout the 4-mo intervention in both groups was 88% of the intended dose (SD = 9%; n = 99) (12). Of the 150 women who completed the supplementation period, 107 mothers (71%) fulfilled the criterion of exclusive breast-feeding for 4 mo. Partly breast-fed children were not excluded from the study, but the degree of breast-feeding was estimated from the intake of infant formula (12).


Figure 1
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  		FIGURE 1  Trial profile illustrating participant flow in the 2 randomized groups (FO or OO) and the HF intake reference group from recruitment from the Danish National Birth Cohort during the randomized intervention period and at the follow-up examinations, with focus on the 7-y follow-up study.

 
    Protocol of the trial. Weight and length at birth were collected from the hospital records and head circumference was measured at a home visit 9 ± 3 d after birth (12). The infants were examined with anthropometric measurements at the age of 2 and 4 mo and at follow-up visits at 9 mo and 2.5 y. Furthermore, breast milk samples were collected at 2, 4, and 9 mo and a blood sample was collected from the mother and the infant at 4 mo to measure the biochemical effect of the intervention by fatty acid analysis of the RBC (12,13). Of the 149 mother-infant pairs who completed the intervention and the 9-mo follow-up, 101 of the children participated in the 2.5-y follow-up, which was performed to assess growth, body composition, blood pressure, heart rate, and immune function of the children [for details, see (13,15)].

    7-y follow-up. These 149 children were also invited to participate in the 7-y follow-up study. Nine of the children were lost to follow-up due to lack of contact, 10 were excluded because they were living too far from the department, and 31 did not wish to participate due to personal reasons. Ninety-nine children agreed to participate in the follow-up study; 1 was excluded because of a broken leg and complete data were collected from the remaining 98 healthy Danish children between November 2006 and February 2007.

    Data collection. Anthropometric measurements were performed on all children by 2 researchers, and no inter-researcher differences were observed. Head, waist, and hip circumference were measured in triplicate with a tape measure (Lasso, Child Growth Foundation). Height was measured in triplicate to 0.1 cm using a portable height measure (Leicester Height Measure, Child Growth Foundation) while children were barefooted. Body weight was measured with children in underwear and socks to 0.1 kg on a calibrated portable digital scale (Tanita WB-100 S MA). Triceps and subscapular skin-fold thickness was measured to 0.1 mm in triplicate with a Harpenden skin-fold caliper (CMS Weighing Equipment) midway between the shoulder and the elbow of the relaxed undominating arm and 2 cm diagonally below the inferior angle of the scapula, respectively. The percentage of body fat was calculated from the sum of triceps- and subscapular skin-fold thickness as follows (16): boys, 1.21 x sum – 0.008 x sum2 – 1.7; girls, 1.33 x sum – 0.013 x sum2 – 2.5. The occurrence of overweight children was based on international age-controlled BMI cut-off values (17).

Blood pressure was measured successfully in all children by the oscillometric principle (18) with a Boso-medicus Prestige unit (Bosch + Sohn) using a 16- to 22-cm cuff (Type CA03). The child was lying on a couch for at least 5 min before and was not allowed to talk during the measurement, except if the measurement were causing discomfort. Three consecutive measurements of systolic (SBP) and diastolic blood pressure (DBP) were made in the lying position in the undominating arm. The mean of the 2nd and 3rd measurements (19) was used and MAP was calculated as DBP + 1/3 x (SBP – DBP).

Diet and physical activity was assessed for 4 consecutive days, Wednesday through Saturday or Sunday through Wednesday, equally distributed between the 3 groups. Dietary data were collected from 93 children using a weighed dietary record and a weight with a resolution of 0.1 g (Soehnle, 8020). The mean daily energy intake (EI) and the intake of nutrients were calculated by Dankost (DK3000, Danish Catering Centre). Physical activity was assessed with a validated position and motion instrument (ActiReg, PreMed AS) (20). Visual onscreen examination was performed during the ActiCalc data processing to ensure that the sensors were positioned correctly during the recording. If the diet or physical activity were recorded for <3 d, on nonconsecutive days, or did not include a weekend day, data were excluded in the analysis. The day was excluded if the ActiReg monitor had been taken off for >3 h. The monitor was not carried at night or during water-based activities and the child and parents were instructed to record the type of activity if the monitor was taken off for >15 min during the day. Metabolic equivalents based on ActiReg approximations were used to assess the energy expenditure during nonwear time. Total energy expenditure was calculated from the ActiReg data and the basal metabolic rate (BMR), estimated from weight, height, age, and sex (21). The physical activity level (PAL = mean daily energy expenditure/BMR) was calculated from the total energy expenditure. Physical activity data were collected from 92 children, 4 of whom had incomplete data (<3 d), leaving 88 children with complete data who were equally distributed between the 3 groups. The pattern of the physical activity was assessed by Habitual Activity Estimated Scale (HAES) questionnaires, which were answered by the parents and the child on 3 of the ActiReg registration days including 1 weekend day. From the questionnaires, we estimated the relative amount of time during 24 h that the child had been inactive (lying), slightly active (sitting), active (standing/walking), or very active (running/jumping).

    Statistics. Data are given as means ± SD or ± SEM for the unadjusted and adjusted mean differences. Nominal variables were compared by {chi}2 analysis and given as ratios. Variables in the ordinal scale and non-Gauss–distributed variables were compared using the Mann-Whitney U test or Kruskal-Wallis test and given as median, 10th–90th percentile. Student's t test or ANOVA were used for group comparisons for all normally distributed continuous variables. The ANOVA of EI, macronutrients, fatty acid distribution, PAL, energy expenditure, and BMR were adjusted for sex, and PAL was also included in the analysis of EI. The ANOVA of body composition were controlled for sex, ponderal index at birth, intake of starch, EI, and PAL. Similar analyses were also performed for weight, height, and head circumference with replacement of the ponderal index at birth with birth weight, length, and head circumference, respectively, and exclusion of starch, EI, and PAL in the models for height and head circumference. The ANOVA of BMI at 2.5 y for children participating in the 7-y follow-up was controlled for sex, ponderal index at birth, as well as EI at 2.5 y. The ANOVA of blood pressure included sex, waist:height ratio, FO supplements after the intervention (yes/no), intake of starch, and PAL. Furthermore, the ANOVA of all outcomes included a sex x intervention interaction, which was excluded in the final model if it was insignificant. If the interaction term was significant, then analyses were performed separately in the gender subgroups. In parametric comparisons, we verified homogeneous variances in the groups and all ANOVA were checked for the absence of heteroscedasticity by an even scatter in the residuals plots. We used Pearson analysis of univariate correlation for associations between the adjusted outcome variables and the DHA content of maternal RBC at the end of the intervention. Correlations between blood pressure and body composition measurements at 2.5 and 7 y and between EI and PAL and energy expenditure at 7 y were also investigated. We used Cooks distance plots to discover potential outliers, but no outliers were observed for any of the outcome variables with a Cook distance > 0.25. All data were analyzed using SPSS for Windows 15.0. With a mean of 32 subjects in each of the 2 randomized groups, this study was powered ({alpha} = 0.05, β = 0.80) to show a raw unadjusted difference of 0.71 SD.


   Results
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
 Results
Discussion
 LITERATURE CITED
 
    Characteristics of the participants. Ninety-eight children participated in the present follow-up study (HF = 34, FO = 36, and OO = 28) (Table 1). The participating and nonparticipating children did not differ with respect to gestational age and weight, length, and head circumference at birth, but the participating children had a higher degree of breast-feeding during the first 4 mo of lactation (P = 0.001). The 3 groups did not differ, except that the FO group tended to have a slightly lower degree of breast-feeding during the intervention period than the OO group (P = 0.072).


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  		TABLE 1 Characteristics of children of mothers randomized to receive FO or OO supplements during lactation and of the HF intake reference group mothers1

 
    Diet and physical activity. The EE and BMR did not differ between the 2 randomized groups (Table 2). However, the unadjusted PAL values tended to differ (P = 0.076) and when adjusted for sex, the PAL of the children in the OO group was higher than that in the FO group. None of the HAES activity categories differed between the randomized groups (Supplemental Table 1). The FO group was in between the HF and OO group for most HAES categories and the relative amount of time that the children were very active was higher in the HF than in the OO group (P = 0.039). The randomized groups did not differ in percentage of EI (E%) from macronutrients, fat quality (Table 2), or in the intake of (n-3) LCPUFA and the ratio of (n-6):(n-3) PUFA (data not shown). The mean dietary (n-6):(n-3) PUFA ratio of the children was 6.1 ± 1.8 and the median (n-3) LCPUFA intake was 0.13 (0.02–0.70) g/d. The mean intake of starch was 81 ± 22 g/d, and when adjusted for sex, it was 15 ± 6 g/d higher in the FO group than in the OO group (P = 0.012). The intakes of sugar, fiber, sodium, potassium, calcium, phosphorus, or other micronutrients did not differ between the randomized groups (the mean nutrient intake is given in Supplemental Table 2). EI was correlated with both the PAL value (r = 0.39; P = 0.003) and energy expenditure (r = 0.59; P < 0.001). When EI was adjusted for PAL, there was an interaction between sex and the intervention and the EI of the boys in the randomized groups differed in the subsequent gender subgroup analyses (P = 0.014), being 1.1 ± 0.4 MJ/d higher in the boys from the FO group. The adjusted EI of the girls in the randomized groups did not differ. The EI of the children in the randomized groups did not correlate with maternal RBC-DHA at 4 mo, but PAL was correlated with maternal RBC-DHA (r = –0.298; P = 0.026; n = 56). This correlation was unaffected by inclusion of the HF group (r = –0.263; P = 0.016; n = 87).


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  		TABLE 2 EI, diet composition, and physical activity at 7 y of children of mothers randomized to receive FO or OO supplements during lactation and of the HF intake reference group mothers1

 
    Body composition. The children in the FO group had larger head circumferences, but this difference was insignificant after adjustment for covariates (Table 3). None of the other anthropometric measures differed between the randomized groups either before or after adjustment. Furthermore, none of the growth or body composition variables were correlated with maternal RBC-DHA either with or without the HF group.


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  		TABLE 3 Body composition of the 7-y-old children of mothers randomized to receive FO or OO supplements during lactation and of the HF intake reference group mothers1

 
The body composition variables at 2.5 and 7 y of age were correlated (BMI, r = 0.63 and P < 0.001; waist:height ratio, r = 0.49 and P < 0.001). Including only children participating in the present follow-up, the BMI at 2.5 y was higher in the FO group than in the OO group both with and without adjustment (n = 49, P = 0.004 and P = 0.002, respectively).

    Blood pressure. The children in the FO group had higher unadjusted mean SBP and MAP than the children in the OO group (Table 4). The blood pressure value for the HF group was between the values of the 2 randomized groups. SBP did not differ between the randomized groups after adjustment for covariates. Due to an interaction between intervention and sex (P = 0.027 for DBP and P = 0.026 for MAP), adjusted ANOVA was performed separately for the 2 sexes. Among the boys, both DBP and MAP differed between the randomized groups, but the blood pressure of the girls did not differ. The adjusted DBP of the 7-y-old children did not correlate with maternal RBC-DHA at 4 mo either in the randomized part of the trial (r = –0.02; P = 0.91; n = 55) or after inclusion of the HF group (r = –0.01; P = 0.93; n = 85). Similar results were found for SBP and MAP.


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  		TABLE 4 Blood pressure of 7-y-old children of mothers randomized to receive F or OO supplements during lactation and of the HF intake reference group mothers1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
 Results
 Discussion
LITERATURE CITED
 
The results presented indicate that the difference in body composition between the randomized groups that was observed at 2.5 y of age (13) had disappeared by the age of 7 y. Overall, our findings agree with the results in the recent 7-y follow-up of the children in the Helland trial, in which there was no correlation between breast-milk DHA and later BMI, but a positive association with the milk content of {alpha}-linolenic acid (22). Previous trials administrating 2–3 g/d of (n-3) LCPUFA during pregnancy and/or lactation or increasing amounts of DHA (up to 1.3 g/d) during lactation have not observed any effect on growth in healthy term infants up to ~2 y of age (10,11,23). One trial in which mothers were supplemented with 0.2 g DHA/d during both pregnancy and lactation (24) reported a lower BMI of the children in the supplemented group at 21 mo of age. In contrast, 4-mo-old, formula-fed male infants supplemented with LCPUFA had a significantly greater weight gain compared with those who were fed a standard infant formula (25). Some animal studies suggest that (n-6) PUFA promotes adipocyte differentiation and that (n-3) PUFA protect against obesity (5,26). However, results of human trials do not support this hypothesis.

We found that BMI was tracking from 2.5 to 7 y. However, because a difference in BMI between the 2 groups was only observed at 2.5 y, we speculate that BMI in the FO group was increasing at a slower rate than that of the OO group. The higher EI among the boys and the lower PAL in the FO group compared with the OO group would be expected to result in a higher BMI in the FO group. Because the difference in body composition was not pronounced, this could indicate that the children in the FO group may be less disposed to overweight. Fish oil has been suggested to enhance energy expenditure (27) and facilitate fat oxidation (28). However, it is also likely that the less-pronounced effect at 7 y could be due to environmental factors blurring the effect of the intervention, such as unhealthy lifestyle, which is complicated to adjust for.

The finding of significantly higher blood pressure of the children in the FO group, especially in the boys, contradicts earlier results in animals and humans (6,7). The observed effect of FO was substantial compared with the long-term effect of breast-feeding, which has been found to reduce SBP by 1–2 mm Hg (29). However, no difference in blood pressure was observed at 2.5 y, but this may be due to intra-individual variation in the blood pressure assessment at that age (15). No association was observed between maternal RBC-DHA and the blood pressure of the children, questioning whether the observed difference in blood pressure was caused by the intervention or was merely a chance finding. Adverse effects of fish oil could in theory be due to toxic oxidation products, which unfortunately was not determined during the intervention. However, microencapsulation should protect the oil against oxidation and the observed increase in maternal RBC (n-3) LCPUFA was as expected with the given dose of fish oil.

The indicated differences in blood pressure, PAL, EI, and starch intake, mainly in boys, could indicate a potential connection between these variables. Diet has in previous studies been linked with blood pressure in both children and adults (30–32). The group differences in PAL, EI, and starch could be due to an unhealthier lifestyle among the boys in the FO group than in the OO group. However, the differences in PAL could also be a true effect of the treatment as indicated by the observed association between 7-y PAL and maternal RBC-DHA at 4 mo. Intake of (n-3) LCPUFA in early life has been suggested to have a programming effect on appetite (33–36). Furthermore, (n-3) LCPUFA has been suggested to have a programming effect on behavior and physical activity (37–39) and investigations are pursuing whether (n-3) LCPUFA intake affects hyperactivity in children with Attention Deficit Hyperactivity Disorder (40). Although not significant in a direct group comparison, the children in the FO group appeared to have more intense activity and possibly more sleep/rest than those in the OO group. The self-reported HAES activity pattern is, however, not very sensitive and a more objective evaluation of the activity pattern and sleep duration is required to be able to investigate the exact nature of the change in activity. These hypotheses of programming effects of (n-3) LCPUFA on human appetite and behavior need further examination before any conclusions can be drawn.

This is the first trial, to our knowledge, to investigate long-term effects on body composition with assessment of diet and PAL. Unfortunately, the assessments of PAL and diet were only done for 4 d and were not completed by all of the children. Furthermore, there is an overall lack of agreement between the EI and energy expenditure of the children. This has also been observed in other studies with children (41) and because there was a good correlation between these two variables, we interpret this as an underreporting of diet in all the children. An assessment of the current (n-3) PUFA status would have improved the study, but this was not financially possible. Despite the long time period between the intervention and the present follow-up, our dropout rate was relatively low (34%). However, the small sample size of the study limits a clear identification of whether or not the maternal FO supplementation had a direct programming effect on blood pressure and body composition in the 7-y-old children. Moreover, not all the infants were exclusively breast-fed during the intervention period and the degree of breast-feeding tended to be higher in the OO group (P = 0.072), which may have limited and blurred the potential effect of the intervention. However, inclusion of breast-feeding as a variable in the ANCOVA model did not significantly affect the results.

The present study raises several new questions of relevance for future research on the health implication of (n-3) PUFA intake: does (n-3) LCPUFA have a long-term negative effect on blood pressure, appetite, and physical activity, and is gender important in this context? The observed potential programming effects on EI and PAL are new and may reflect a general central nervous system effect. The potential negative programming effects on blood pressure may be a chance finding, but our results indicate possible adverse effects among the 7-y-old children, especially the boys, which contradict the current hypothesis of a long-term, health-improving effect of the early (n-3) LCPUFA intake. Thus, further studies are needed to investigate the potential long-term effect and their implications for overall health and well-being.


   ACKNOWLEDGMENTS
 
We thank Berit Worm Rothausen for her assistance with the ActiReg-equipment.


   FOOTNOTES
 
1 Supported by FØTEK, The Danish Research and Development Program for Food and Technology and BASF Aktiengesellschaft. Back

2 Author disclosures: M. Asserhøj, S. Nehammer, J. Matthiessen, K. F. Michaelsen, and L. Lauritzen, no conflicts of interest. Back

3 Supplemental Tables 1 and 2 are available with the online posting of this paper at jn.nutrition.org. Back

6 Abbreviations used: BMR, basal metabolic rate; DBP, diastolic blood pressure; DHA, docosahexaenoic acid; EI, energy intake; FO, fish oil treatment group; HF, high-fish–intake group; LCPUFA, long-chain PUFA; MAP, mean arterial pressure; OO, olive oil treatment group; PAL, physical activity level; SBP, systolic blood pressure. Back

Manuscript received 9 July 2008. Initial review completed 21 August 2008. Revision accepted 18 November 2008.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
 Results
 Discussion
 LITERATURE CITED
 

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