http://informahealthcare.com/ijf ISSN: 0963-7486 (print), 1465-3478 (electronic) Int J Food Sci Nutr, 2014; 65(3): 268–272 ! 2014 Informa UK Ltd. DOI: 10.3109/09637486.2013.854744
FOOD AND NUTRITION SURVEYS
Maternal dietary counseling during pregnancy and infant fatty acid profiles Katri Niinivirta1,2, Pa¨ivi Laakso3, Kaisa Linderborg4, Tuija Poussa5, Erika Isolauri2, and Kirsi Laitinen1,6 1
The Functional Foods Forum, University of Turku, Turku, Finland, 2Department of Pediatrics, Turku University Hospital and University of Turku, Turku, Finland, 3Eurofins Scientific Finland Oy, Raisio, Finland, 4Department of Biochemistry, University of Turku, Turku, Finland, 5Stat-Consulting, Nokia, Finland, and 6Institute of Biomedicine, University of Turku, Turku, Finland
Abstract
Keywords
We aimed to explore whether maternal dietary counseling to increase the intake of unsaturated fatty acids (FA) is reflected in infant FA status. Serum cholesteryl ester (CE) and triacylglycerol (TAG) FA were analyzed from infants of 45 women randomized to receive dietary counseling from the first trimester of pregnancy and 45 control women. Counseling resulted in a higher intake of polyunsaturated FA and a lower intake of saturated FA. The dietary intake was reflected in cord blood TAGs: the n6 to n3 FA ratio was lower [mean difference 0.50 (95%CI 0.95 to 0.06)] and the sum of n3 FA was higher in the intervention than in the control group [1.46 (0.44 to 2.48)% of total FA]. Reasons for the lack of changes in the cord blood CE fraction and FA fractions at 1-month remain unclear, but may indicate that the changes achieved in the maternal diet through counseling were too modest.
Diet, fetal blood, polyunsaturated fatty acids, pregnant women, randomized controlled trial
Nutrition in fetal life and early infancy may modify metabolism and thus induce lifetime effects on health. Relative overload of dietary n6 to n3 polyunsaturated fatty acids (PUFA) has been implicated in the rising allergy prevalence in Westernized countries (Calder, 2006). Previous research is controversial in terms of PUFA supplementation to clinical effects (Kremmyda et al., 2011), thus the optimal balance and methods to improve n6 to n3 relation during pregnancy and lactation remain unknown. Increasing infant’s dietary PUFA supply results in beneficial changes in lipid metabolism, for example lower cholesterol levels (Agostoni et al., 1994; Mize et al., 1995). The developing fetus depends on the mother for fatty acid (FA) supply (Vlaardingerbroek & Hornstra, 2004), and so does the breastfed newborn. Thus, changing the composition of the mother’s dietary FA intake may also offer at an early stage a way to modify fetal and neonatal FA status (Noakes et al., 2012) with possible longterm health effects. To evaluate this possibility, we targeted infants at risk due to their family history of allergy. We chose to use an approach applicable to public health: the dietary counseling of mothers. The counseling aimed to modify the quality and quantity of dietary fat to increase the intake of unsaturated FA and decrease that of saturated FA. Previously, we demonstrated a benefit of maternal dietary counseling to the newborn as a reduction in biochemical markers for essential FA deficiency as measured in phospholipid (PL) FA (Niinivirta et al., 2011). In the present study, we aimed to further evaluate the impact of
Correspondence: Katri Niinivirta, Functional Foods Forum, 20014 University of Turku, Finland. Tel: +358 2 333 6822. Fax: +358 2 333 6862. E-mail: [email protected]
Received 6 May 2013 Revised 7 October 2013 Accepted 9 October 2013 Published online 13 November 2013
modifying maternal diet through counseling on both short- and long-term markers of infant FA metabolism, namely, triacylglycerol (TAG) and cholesteryl ester (CE) FA.
Subjects and methods Study population and design The present study is part of a prospective mother–infant nutrition and probiotic study (NCT00167700, section 3; http://www.clinicaltrials.gov), which aims to optimize maternal dietary intake and metabolism to advance maternal health and thereby possibly reduce the risk of disease in the child. In brief, pregnant women from allergic risk families (mother, father or sibling of the unborn child with allergic disease) at less than 17 weeks’ gestation were recruited (Niinivirta et al., 2011). The mothers’ atopic status was tested by skin prick test at the third trimester of pregnancy. For the present study aim, 45 mother–children pairs from a dietary counseling group with placebo and 45 pairs from a control group with placebo were taken to an FA analysis in consecutive order of recruitment. The composition and concentration of serum CE and TAG FA were analyzed from cord blood and from blood sampled at 1 month of age. Written informed consent was obtained from the mothers before enrollment. The study complies with the Declaration of Helsinki as revised in 2000, and the Ethical Committee of the Hospital District of Southwest Finland has approved the study.
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Introduction
History
Dietary intervention The intervention group received dietary counseling at each trimester and 1-month postpartum by a nutritionist, aiming at a diet complying with that which was recommended (Piirainen et al., 2006). Special attention was given to the quality and
Maternal diet and infant fatty acid profiles
DOI: 10.3109/09637486.2013.854744
quantity of dietary fat, with the intention of increasing the intake of unsaturated FA and reducing that of saturated FA (Piirainen et al., 2006). The recommended amounts of foods were planned to result in monounsaturated fatty acids (MUFA) contributing 10–15% of the total daily energy intake (E %), PUFA contributing 5–10 E%, and SFA contributing 10 E%. Total intake of fat was aimed for 30 E%, carbohydrates 55–60 E%, and protein 10–15 E%. Daily food products with favorable fat compositions (e.g. low-erucic acid rapeseed oil-based spreads and salad dressings) were provided for use at home to support compliance to the recommended diet. Practical dietary advice was adjusted to the women’s current dietary habits and food diary analysis. All women also attended municipal well-women clinics for health checkups and counseling. As previously reported in detail (Niinivirta et al., 2011; Piirainen, et al., 2006), dietary counseling resulted in statistically significantly higher intakes of PUFA and lower intakes of saturated FA in the counseling than in the control group as analyzed from 3-d food diaries. Daily intakes of energy and nutrients were calculated using Micro-Nutrica computerprogram (version 2.5; Research Centre of the Social Insurance Institution, Turku, Finland).
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Table 1. Clinical characteristics of women and their infants in the dietary intervention and control groupsa. Intervention (n ¼ 45)
Control (n ¼ 45)
Maternal characteristics Age (y) College or university degree Smoking during pregnancy Primigravida Allergic disease Skin prick test positive* Pre-pregnancy BMI (kg/m2) Weight gain during pregnancy (kg)
30.8 5.4 31 (68.9) 3 (6.8) 21 (46.7) 36 (80.0) 23 (52.3) 24.2 4.2 15.2 5.0
30.0 4.4 36 (80.0) 2 (4.5) 25 (55.6) 36 (80.0) 24 (54.5) 23.1 3.4 14.8 5.2
Infant characteristics Birth at weeks of gestation Birth weight (g) Birth length (cm) Head circumference (cm) Exclusively breastfed at 1 mo
39.7 2.1 3610 480 51.3 1.7 35.2 1.3 29 (74.4)
40.0 1.4 3590 520 50.8 2.2 35.1 1.3 30 (83.3)
a
Values are mean SD, or n (%). *Skin prick test results were obtained from 44 mothers in the intervention and control group.
Fatty acid analyses FA were analyzed from infants’ cord blood and venous blood samples at 1-month of age, when blood was drawn from the antecubital vein after topical lidocain anesthesia by a trained nursing staff at Turku University Hospital. FA composition and concentration of serum TAG and CE were analyzed by gas chromatography after solid phase extraction of the lipids. The quantification of TAG and CE in serum lipid fractions was based on internal standards triheneicosanoin (Larodan AB, Malmo¨, Sweden), heptadecanoylcholesterol and dinonadecanoylphosphatidylcholine (Sigma-Aldrich, St-Louis, MO), respectively. The details of the analysis protocol have been described earlier (Niinivirta et al., 2011). Statistical analyses The distributions of variables were checked using graphical plots, which indicated that departures from normal distribution were not too marked for parametric analysis. FA at birth and at 1 month of age were analyzed using the independent-samples t-test and the analysis of variance for repeated measures (rmANOVA), in which the factors were group (intervention versus control), time and group time interaction. The two-way ANOVA (with interaction term) was used to study the potential role of maternal skin prick test as an effect modifier. FA are presented as means (SD) with 95% confidence intervals (CI). p Values less than 0.05 were considered to be statistically significant for a two-sided test. SPSS version 16.0 was used for all statistical analyses (SPSS Inc., Chicago, IL).
Results Characteristics of subjects The children were born at a mean gestational age of 39.9 weeks (range 30.3–42.1), except for three preterm deliveries (30.3, 34.9 and 35.6 weeks). The mean length was 51.0 (44.0–55.0) cm and weight 3600 (1630–4660) g at birth. Only one child was without breastfeeding of any kind at 1 month of age. The detailed clinical characteristics of the subjects are provided in Table 1. The impact of dietary counseling on proportions (%) of serum FA Significant differences between dietary counseling and control groups in FA in TAG fraction were observed; the proportion of
saturated FA was lower [mean difference 1.31 (95% CI 2.59 to 0.04), p ¼ 0.043], the sum of n3 FA was higher [mean difference 0.99 (95% CI 0.23 to 1.74), p ¼ 0.012], and the ratio of n6 to n3 FA was lower [0.76 (1.40 to 0.12), p ¼ 0.022) over the study period from cord blood to 1-month in children whose mothers were receiving versus not receiving counseling (rmANOVA, group effect). To further investigate these group differences, FA compositions were compared between the groups in cord blood and 1-month samples separately (Table 2). Significant differences between groups were observed in cord blood TAG, the sum of n3 FA was higher in the counseling group (p ¼ 0.006) and the sum of SFA and the n6 and n3 FA ratio were lower in the counseling group (p ¼ 0.043 and p ¼ 0.029, respectively). There were no differences between the groups in TAG FA in 1-month samples (Table 2). The group differences were not significant in CE FA in either time point (Table 3). The impact of dietary counseling on concentrations (mg/ L) of serum FA The concentration of eicosapentaenoic acid (20:5n3, EPA) in TAG (Table 4) was statistically significantly increased from cord blood to 1-month in children whose mothers received dietary counseling, but declined in control subjects (time group interaction p ¼ 0.009; rmANOVA). When evaluating the two time points separately, the dietary counseling had no effect on FA concentrations in cord blood or 1-month in TAG (Table 4) or CE (Table 5) fractions.
Discussion Maternal dietary counseling ensuing heightened intakes of PUFA and lowered intakes of SFA was reflected in FA composition of cord serum as an increased proportion of n3 FA and reduced proportion of SFA in TAG fraction. Our findings confirm the delivery of maternal dietary changes during pregnancy to the infant, the TAG FA representing a biomarker of exposure to exogenous FA over a very recent period of dietary intake (Lagstro¨m et al., 1998). The modification of infant’s FA status at an early stage may be of importance and carry long-term health benefits up to adulthood (Barman et al., 2013; Kaikkonen et al., 2012).
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Table 2. Serum triacylglycerol fatty acids as proportion (%) of the total fatty acids from cord and 1-month samples in the intervention and the control groupsa. Cord blood
1-month
Intervention (n ¼ 31) Control (n ¼ 28) Mean Mean SD Mean SD difference Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n 3 22:6n3b Sum n3 n6/n3
34.91 2.27 41.52 3.62 23.58 3.95 9.89 1.79 0.49 0.13 0.83 0.16 3.49 0.99 0.60 0.17 0.86 0.26 16.16 2.60 0.65 0.22 0.85 0.45 0.60 0.32 1.47 0.50 6.53 2.45 2.72 0.81
36.22 2.61 42.02 3.28 21.76 3.53 9.59 2.34 0.50 0.18 0.85 0.31 3.22 0.88 0.57 0.14 0.85 0.30 15.58 2.93 0.62 0.23 0.78 0.34 0.47 0.18 1.29 0.37 5.08 1.32 3.22 0.91
1.31 0.50 1.81 0.30 0.01 0.02 0.27 0.03 0.01 0.58 0.03 0.06 0.13 0.18 1.46 0.50
95% CI 2.59, 2.31, 0.15, 0.78, 0.09, 0.15, 0.22, 0.05, 0.13, 0.86, 0.09, 0.15, 0.00, 0.05, 0.44, 0.95,
0.04* 1.31 3.78 1.38 0.07 0.11 0.76 0.12 0.16 2.02 0.15 0.27 0.26 0.41 2.48* 0.06*
Intervention (n ¼ 33) Control (n ¼ 31) Mean Mean SD Mean SD difference 35.42 4.25 47.19 2.69 17.39 2.38 12.40 2.27 0.17 0.10 0.35 0.11 0.94 0.32 0.12 0.05 0.08 0.06 14.06 2.10 1.67 0.47 0.29 0.20 0.26 0.14 0.78 0.45 3.01 1.02 5.29 2.33
36.10 3.26 46.97 3.26 16.93 2.97 12.09 2.72 0.17 0.11 0.36 0.12 0.94 0.31 0.14 0.07 0.10 0.10 13.79 2.82 1.48 0.44 0.25 0.23 0.26 0.11 0.76 0.47 2.75 0.83 5.44 1.90
0.68 0.22 0.46 0.31 0.00 0.01 0.01 0.01 0.02 0.27 0.19 0.04 0.00 0.02 0.26 0.15
95% CI 2.58, 1.27, 0.88, 0.94, 0.06, 0.07, 0.15, 0.04, 0.06, 0.97, 0.04, 0.07, 0.06, 0.21, 0.21, 1.22,
1.22 1.71 1.80 1.56 0.05 0.05 0.16 0.02 0.02 1.50 0.42 0.15 0.07 0.25 0.73 0.91
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses. *p50.05.
b
Table 3. Serum cholesterol ester fatty acids as proportion (%) of the total fatty acids from cord and 1-month samples in the intervention and the control groupsa. Cord blood
Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n 6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n3 22:6n3b Sum n3 n6/n3
1 month
Intervention (n ¼ 31) Mean SD
Control (n ¼ 28) Mean SD
Mean difference
24.0 2.0 42.3 4.7 33.7 4.8 16.2 2.0 0.72 0.24 1.45 0.23 12.1 2.8 0.01 0.03 0.15 0.17 30.6 4.4 0.28 0.18 0.85 0.40 0.04 0.12 1.47 0.50 2.65 0.8 12.4 3.1
24.2 1.2 42.1 4.0 33.7 4.2 16.3 2.8 0.78 0.23 1.48 0.43 12.0 2.2 0.02 0.1 0.11 0.13 30.6 4.2 0.28 0.16 0.80 0.31 0.01 0.04 1.29 0.37 2.38 0.7 13.7 3.8
0.21 0.21 0.00 0.10 0.06 0.02 0.13 0.01 0.03 0.03 0.00 0.06 0.03 0.18 0.26 1.36
95% CI 1.05, 2.08, 2.34, 1.38, 0.18, 0.20, 1.20, 0.05, 0.05, 2.25, 0.09, 0.13, 0.02, 0.05, 0.14, 3.18,
0.63 2.49 2.35 1.18 0.06 0.16 1.47 0.03 0.11 2.20 0.09 0.25 0.08 0.41 0.67 0.46
Intervention (n ¼ 33) Mean SD
Control (n ¼ 31) Mean SD
Mean difference
19.0 2.0 34.2 2.9 46.8 3.5 36.7 3.6 0.45 0.11 0.78 0.17 6.32 1.73 0.00 0.01 0.09 0.10 44.3 3.5 0.66 0.20 0.70 0.41 0.03 0.03 0.70 0.23 2.08 0.73 24.4 10.6
19.4 1.7 34.6 3.5 46.0 4.2 36.0 3.9 0.48 0.16 0.80 0.16 6.25 1.61 0.00 0.01 0.08 0.09 43.6 4.3 0.58 0.17 0.68 0.35 0.02 0.04 0.70 0.21 1.98 0.50 23.5 6.5
0.39 0.39 0.79 0.68 0.02 0.02 0.07 0.00 0.01 0.72 0.08 0.02 0.01 0.00 0.10 0.91
95% CI 1.32, 2.01, 1.13, 1.19, 0.09, 0.11, 0.77, 0.01, 0.04, 1.22, 0.02, 0.17, 0.01, 0.10, 0.21, 3.53,
0.54 1.23 2.71 2.55 0.05 0.06 0.91 0.01 0.06 2.66 0.17 0.21 0.02 0.11 0.42 5.34
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses.
b
Dietary counseling, an approach applicable to public health setting, resulted in increased intakes of n3 FA in the intervention group over the entire course of pregnancy and lactation, also reported previously in the larger study population (Ilmonen et al., 2011; Piirainen et al., 2006) Continuous supply of FA from the usual diet was ensured through supporting dietary counseling with provision of rapeseed oil based food products from early pregnancy onwards. This approach was evaluated feasible to induce health-benefits in both mother and child, as women of childbearing age possess a capacity for ALA conversion to longer chain derivatives like DHA and EPA (Burdge & Wootton, 2002). Further, we have previously demonstrated the impact of maternal dietary counseling in improving markers of essential FA and functional DHA status in cord blood PL FA (Niinivirta et al., 2011). Thus, we expected to demonstrate changes also in the lipid
fractions reflecting shorter-term dietary intake, namely, in TAG and CE fractions. In previous studies both TAG and CE FA have been successfully used as biomarkers for dietary intake in adults (Baylin & Campos, 2006) and children (Lagstro¨m et al., 1998; Moilanen et al., 1983; Nikkari et al., 1983), but to our knowledge there is no data on the impact of maternal dietary modification on infant TAG and CE FA. Previous intervention studies during pregnancy have usually analyzed PL FA as markers for dietary FA intake (de Groot et al., 2004; Helland et al., 2001, 2006; KraussEtschmann et al., 2007). While PL FA represent a time period of weeks to months, CE are considered to reflect consumption from a few days to 1–2 weeks and TAG from the last few days (Hodson et al., 2008; Zock et al., 1997). Our results suggest that TAG FA might be used as markers of infant FA supply through maternal diet during pregnancy.
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Table 4. Serum triacylglycerol fatty acids as concentration (mg/L) from cord and 1-month samples in the intervention and the control groupsa. Cord blood
Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n3 22:6n3b Sum n3
1-month
Intervention (n ¼ 31) Mean SD
Control (n ¼ 28) Mean SD
Mean difference
9.10 4.87 10.79 5.68 6.29 3.73 2.69 1.69 0.13 0.08 0.22 0.13 0.95 0.68 0.17 0.13 0.23 0.16 4.38 2.76 0.18 0.12 0.20 0.12 0.17 0.13 1.13 0.71 1.68 1.02
12.22 11.47 13.98 12.69 7.50 7.14 3.52 3.83 0.16 0.16 0.30 0.36 1.04 0.95 0.20 0.20 0.29 0.29 5.50 5.61 0.22 0.22 0.23 0.15 0.17 0.17 1.03 0.83 1.65 1.33
3.12 3.18 1.21 0.83 0.03 0.08 0.10 0.03 0.05 1.12 0.05 0.02 0.01 0.10 0.03
95% CI 7.87, 8.47, 4.26, 2.42, 0.10, 0.23, 0.52, 0.12, 0.18, 3.49, 0.14, 0.09, 0.09, 0.30, 0.59,
1.62 2.10 1.83 0.76 0.04 0.07 0.33 0.05 0.07 1.25 0.05 0.05 0.07 0.51 0.64
Intervention (n ¼ 33) Mean SD
Control (n ¼ 31) Mean SD
Mean difference
34.25 16.57 45.75 21.80 16.85 8.65 12.24 6.74 0.14 0.06 0.32 0.17 0.85 0.43 0.11 0.06 0.07 0.05 13.73 7.21 1.64 1.01 0.24 0.17 0.24 0.17 0.70 0.53 2.81 1.67
32.73 13.88 42.28 16.48 15.29 6.51 11.06 5.11 0.14 0.06 0.31 0.15 0.81 0.35 0.12 0.07 0.09 0.09 12.54 5.57 1.38 0.71 0.17 0.10 0.22 0.10 0.62 0.37 2.39 1.05
1.52 3.47 1.56 1.18 0.00 0.01 0.04 0.01 0.02 1.19 0.26 0.06 0.02 0.08 0.42
95% CI 6.14, 6.23, 2.28, 1.82, 0.03, 0.07, 0.16, 0.04, 0.06, 2.04, 0.18, 0.00, 0.05, 0.15, 0.28,
9.18 13.18 5.41 4.18 0.03 0.09 0.23 0.02 0.01 4.43 0.70 0.13 0.09 0.31 1.12
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses.
b
Table 5. Serum cholesteryl ester fatty acids as concentration (mg/L) from cord and 1-month samples in the intervention and the control groupsa. Cord blood
Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n3 22:6n3b Sum n3
1-month
Intervention (n ¼ 31) Mean SD
Control (n ¼ 28) Mean SD
Mean difference
16.78 5.82 29.41 9.97 23.31 8.40 11.22 4.04 0.49 0.21 1.00 0.34 8.36 3.44 0.01 0.02 0.01 0.11 21.17 7.71 0.19 0.12 0.59 0.33 0.02 0.06 1.02 0.51 1.83 0.81
16.57 5.56 28.81 10.57 22.79 7.22 10.93 3.53 0.52 0.20 1.02 0.42 8.13 3.02 0.02 0.09 0.08 0.09 20.69 6.73 0.19 0.11 0.53 0.23 0.01 0.03 0.88 0.38 1.61 0.62
0.21 0.60 0.51 0.30 0.03 0.02 0.22 0.01 0.02 0.47 0.01 0.06 0.02 0.14 0.22
95% CI 2.77, 4.76, 3.59, 1.69, 0.14, 0.22, 1.47, 0.04, 0.03, 3.32, 0.05, 0.09, 0.01, 0.10, 0.16,
3.18 5.96 4.62 2.28 0.07 0.18 1.92 0.02 0.07 4.26 0.07 0.20 0.04 0.38 0.60
Intervention (n ¼ 33) Mean SD
Control (n ¼ 31) Mean SD
Mean difference
24.86 8.44 44.97 14.52 61.33 19.64 48.06 15.57 0.58 0.20 1.02 0.40 8.31 3.62 0.00 0.01 0.13 0.02 58.09 18.64 0.87 0.40 0.91 0.60 0.03 0.05 0.41 0.07 2.73 1.30
27.00 7.72 48.37 14.35 63.85 16.58 50.03 13.50 0.65 0.22 1.09 0.29 8.62 2.91 0.00 0.02 0.12 0.02 60.50 15.78 0.83 0.39 0.94 0.54 0.03 0.05 0.40 0.07 2.77 1.05
2.14 3.40 2.52 1.97 0.07 0.07 0.31 0.00 0.01 2.41 0.04 0.03 0.01 0.05 0.04
95% CI 6.19, 10.62, 11.63, 9.27, 0.17, 0.24, 1.94, 0.01, 0.06, 11.07, 0.16, 0.31, 0.02, 0.26, 0.63,
1.91 3.82 6.59 5.33 0.04 0.10 1.33 0.01 0.07 6.25 0.23 0.26 0.03 0.15 0.56
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses.
b
Although the detected changes in cord blood TAG FA were as expected, no effect by the maternal dietary intervention in CE FA was observed. One apparent reason for the lack of effect is related to the magnitude of change in the dietary FA content achieved through counseling. Although the change was evident, it remained modest compared for example to a recent dietary intervention study providing fish (salmon) to expecting mothers (Miles et al., 2011). The change in blood lipid FA is clearly related to the dose of FA administered, as demonstrated by several studies using fish oil supplements (Brown et al., 1990; Harris et al., 1983). In a similar way, the effect ensuing to the infant has been demonstrated in previous intervention studies using FA supplements to the mother (Helland et al., 2006; Jensen et al., 2000; Krauss-Etschmann et al., 2007). In the present study, no changes were observed in FA status at 1 month of age, although maternal dietary changes as well as modification of breast milk FA composition following the dietary counseling was verified (Hoppu et al., 2012). In the breast milk of the mothers receiving counseling, the proportion of a-linolenic acid (ALA, 18:3n3)
and total n3 FA increased and the ratio of n6/n3 FA was decreased compared to the control women (Hoppu et al., 2012). This further supports the notion that more intense dietary changes are required to induce FA status modification of the infant, particularly during the post-natal period. Moreover, when interpreting the results, some biological aspects of FA metabolism during pregnancy and breastfeeding need to be taken in consideration. Firstly, dietary FA might be utilized by maternal metabolism: FA are incorporated into cell membranes in tissues and particularly long-chain PUFA act as substrates for synthesis of eicosanoids (Sala-Vila et al., 2008). This is relevant particularly during pregnancy and lactation, because the metabolic demand of FA is increased. Secondly, selective placental fatty acid transfer (biomagnification) during gestation (Haggarty, 2010) could level the possible differences between different dietary intakes at time of birth and thus between study groups. Further, modification of FA by dietary counseling is challenging in this population of well-nourished and welleducated women, who already present with relatively high
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proportions of unsaturated FA in the diet or in the body. Naturally, a larger sample size might be of help in demonstrating differences between the study groups in further studies.
Conclusions Our results suggest that cord blood TAG FA may be used as dietary markers of infant FA status reflecting a change in maternal diet. Early modification of infant’s FA status by increasing the proportion of unsaturated FA, particularly n3 FA, may be of importance both in the short (Kremmyda et al., 2011) and long term, benefits possibly extending up to adulthood (Barman et al., 2013; Kaikkonen et al., 2012). However, as no changes in the CE FA or FA at 1 month of age were detected, it may be speculated that more drastic measures, such as supplementation of FA, in either maternal or infant diet may be necessary.
Acknowledgements We would like to thank Ulla-Maija Eriksson for her clinical work with the study participants and Patrick Gallagher for the grammatical review of the article. Provision of food products was by Raisio plc (Raisio, Finland).
Declaration of interest This work was supported in part by a grant from the Social Insurance Institution of Finland, the Academy of Finland, the Yrjo¨ Jahnsson Foundation and a personal grant from the Maud Kuistila Memorial Foundation for KN. The authors declare no conflicts of interests. The authors alone are responsible for the content and writing of this article.
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FOOD AND NUTRITION SURVEYS
Maternal dietary counseling during pregnancy and infant fatty acid profiles Katri Niinivirta1,2, Pa¨ivi Laakso3, Kaisa Linderborg4, Tuija Poussa5, Erika Isolauri2, and Kirsi Laitinen1,6 1
The Functional Foods Forum, University of Turku, Turku, Finland, 2Department of Pediatrics, Turku University Hospital and University of Turku, Turku, Finland, 3Eurofins Scientific Finland Oy, Raisio, Finland, 4Department of Biochemistry, University of Turku, Turku, Finland, 5Stat-Consulting, Nokia, Finland, and 6Institute of Biomedicine, University of Turku, Turku, Finland
Abstract
Keywords
We aimed to explore whether maternal dietary counseling to increase the intake of unsaturated fatty acids (FA) is reflected in infant FA status. Serum cholesteryl ester (CE) and triacylglycerol (TAG) FA were analyzed from infants of 45 women randomized to receive dietary counseling from the first trimester of pregnancy and 45 control women. Counseling resulted in a higher intake of polyunsaturated FA and a lower intake of saturated FA. The dietary intake was reflected in cord blood TAGs: the n6 to n3 FA ratio was lower [mean difference 0.50 (95%CI 0.95 to 0.06)] and the sum of n3 FA was higher in the intervention than in the control group [1.46 (0.44 to 2.48)% of total FA]. Reasons for the lack of changes in the cord blood CE fraction and FA fractions at 1-month remain unclear, but may indicate that the changes achieved in the maternal diet through counseling were too modest.
Diet, fetal blood, polyunsaturated fatty acids, pregnant women, randomized controlled trial
Nutrition in fetal life and early infancy may modify metabolism and thus induce lifetime effects on health. Relative overload of dietary n6 to n3 polyunsaturated fatty acids (PUFA) has been implicated in the rising allergy prevalence in Westernized countries (Calder, 2006). Previous research is controversial in terms of PUFA supplementation to clinical effects (Kremmyda et al., 2011), thus the optimal balance and methods to improve n6 to n3 relation during pregnancy and lactation remain unknown. Increasing infant’s dietary PUFA supply results in beneficial changes in lipid metabolism, for example lower cholesterol levels (Agostoni et al., 1994; Mize et al., 1995). The developing fetus depends on the mother for fatty acid (FA) supply (Vlaardingerbroek & Hornstra, 2004), and so does the breastfed newborn. Thus, changing the composition of the mother’s dietary FA intake may also offer at an early stage a way to modify fetal and neonatal FA status (Noakes et al., 2012) with possible longterm health effects. To evaluate this possibility, we targeted infants at risk due to their family history of allergy. We chose to use an approach applicable to public health: the dietary counseling of mothers. The counseling aimed to modify the quality and quantity of dietary fat to increase the intake of unsaturated FA and decrease that of saturated FA. Previously, we demonstrated a benefit of maternal dietary counseling to the newborn as a reduction in biochemical markers for essential FA deficiency as measured in phospholipid (PL) FA (Niinivirta et al., 2011). In the present study, we aimed to further evaluate the impact of
Correspondence: Katri Niinivirta, Functional Foods Forum, 20014 University of Turku, Finland. Tel: +358 2 333 6822. Fax: +358 2 333 6862. E-mail: [email protected]
Received 6 May 2013 Revised 7 October 2013 Accepted 9 October 2013 Published online 13 November 2013
modifying maternal diet through counseling on both short- and long-term markers of infant FA metabolism, namely, triacylglycerol (TAG) and cholesteryl ester (CE) FA.
Subjects and methods Study population and design The present study is part of a prospective mother–infant nutrition and probiotic study (NCT00167700, section 3; http://www.clinicaltrials.gov), which aims to optimize maternal dietary intake and metabolism to advance maternal health and thereby possibly reduce the risk of disease in the child. In brief, pregnant women from allergic risk families (mother, father or sibling of the unborn child with allergic disease) at less than 17 weeks’ gestation were recruited (Niinivirta et al., 2011). The mothers’ atopic status was tested by skin prick test at the third trimester of pregnancy. For the present study aim, 45 mother–children pairs from a dietary counseling group with placebo and 45 pairs from a control group with placebo were taken to an FA analysis in consecutive order of recruitment. The composition and concentration of serum CE and TAG FA were analyzed from cord blood and from blood sampled at 1 month of age. Written informed consent was obtained from the mothers before enrollment. The study complies with the Declaration of Helsinki as revised in 2000, and the Ethical Committee of the Hospital District of Southwest Finland has approved the study.
20 14
Introduction
History
Dietary intervention The intervention group received dietary counseling at each trimester and 1-month postpartum by a nutritionist, aiming at a diet complying with that which was recommended (Piirainen et al., 2006). Special attention was given to the quality and
Maternal diet and infant fatty acid profiles
DOI: 10.3109/09637486.2013.854744
quantity of dietary fat, with the intention of increasing the intake of unsaturated FA and reducing that of saturated FA (Piirainen et al., 2006). The recommended amounts of foods were planned to result in monounsaturated fatty acids (MUFA) contributing 10–15% of the total daily energy intake (E %), PUFA contributing 5–10 E%, and SFA contributing 10 E%. Total intake of fat was aimed for 30 E%, carbohydrates 55–60 E%, and protein 10–15 E%. Daily food products with favorable fat compositions (e.g. low-erucic acid rapeseed oil-based spreads and salad dressings) were provided for use at home to support compliance to the recommended diet. Practical dietary advice was adjusted to the women’s current dietary habits and food diary analysis. All women also attended municipal well-women clinics for health checkups and counseling. As previously reported in detail (Niinivirta et al., 2011; Piirainen, et al., 2006), dietary counseling resulted in statistically significantly higher intakes of PUFA and lower intakes of saturated FA in the counseling than in the control group as analyzed from 3-d food diaries. Daily intakes of energy and nutrients were calculated using Micro-Nutrica computerprogram (version 2.5; Research Centre of the Social Insurance Institution, Turku, Finland).
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Table 1. Clinical characteristics of women and their infants in the dietary intervention and control groupsa. Intervention (n ¼ 45)
Control (n ¼ 45)
Maternal characteristics Age (y) College or university degree Smoking during pregnancy Primigravida Allergic disease Skin prick test positive* Pre-pregnancy BMI (kg/m2) Weight gain during pregnancy (kg)
30.8 5.4 31 (68.9) 3 (6.8) 21 (46.7) 36 (80.0) 23 (52.3) 24.2 4.2 15.2 5.0
30.0 4.4 36 (80.0) 2 (4.5) 25 (55.6) 36 (80.0) 24 (54.5) 23.1 3.4 14.8 5.2
Infant characteristics Birth at weeks of gestation Birth weight (g) Birth length (cm) Head circumference (cm) Exclusively breastfed at 1 mo
39.7 2.1 3610 480 51.3 1.7 35.2 1.3 29 (74.4)
40.0 1.4 3590 520 50.8 2.2 35.1 1.3 30 (83.3)
a
Values are mean SD, or n (%). *Skin prick test results were obtained from 44 mothers in the intervention and control group.
Fatty acid analyses FA were analyzed from infants’ cord blood and venous blood samples at 1-month of age, when blood was drawn from the antecubital vein after topical lidocain anesthesia by a trained nursing staff at Turku University Hospital. FA composition and concentration of serum TAG and CE were analyzed by gas chromatography after solid phase extraction of the lipids. The quantification of TAG and CE in serum lipid fractions was based on internal standards triheneicosanoin (Larodan AB, Malmo¨, Sweden), heptadecanoylcholesterol and dinonadecanoylphosphatidylcholine (Sigma-Aldrich, St-Louis, MO), respectively. The details of the analysis protocol have been described earlier (Niinivirta et al., 2011). Statistical analyses The distributions of variables were checked using graphical plots, which indicated that departures from normal distribution were not too marked for parametric analysis. FA at birth and at 1 month of age were analyzed using the independent-samples t-test and the analysis of variance for repeated measures (rmANOVA), in which the factors were group (intervention versus control), time and group time interaction. The two-way ANOVA (with interaction term) was used to study the potential role of maternal skin prick test as an effect modifier. FA are presented as means (SD) with 95% confidence intervals (CI). p Values less than 0.05 were considered to be statistically significant for a two-sided test. SPSS version 16.0 was used for all statistical analyses (SPSS Inc., Chicago, IL).
Results Characteristics of subjects The children were born at a mean gestational age of 39.9 weeks (range 30.3–42.1), except for three preterm deliveries (30.3, 34.9 and 35.6 weeks). The mean length was 51.0 (44.0–55.0) cm and weight 3600 (1630–4660) g at birth. Only one child was without breastfeeding of any kind at 1 month of age. The detailed clinical characteristics of the subjects are provided in Table 1. The impact of dietary counseling on proportions (%) of serum FA Significant differences between dietary counseling and control groups in FA in TAG fraction were observed; the proportion of
saturated FA was lower [mean difference 1.31 (95% CI 2.59 to 0.04), p ¼ 0.043], the sum of n3 FA was higher [mean difference 0.99 (95% CI 0.23 to 1.74), p ¼ 0.012], and the ratio of n6 to n3 FA was lower [0.76 (1.40 to 0.12), p ¼ 0.022) over the study period from cord blood to 1-month in children whose mothers were receiving versus not receiving counseling (rmANOVA, group effect). To further investigate these group differences, FA compositions were compared between the groups in cord blood and 1-month samples separately (Table 2). Significant differences between groups were observed in cord blood TAG, the sum of n3 FA was higher in the counseling group (p ¼ 0.006) and the sum of SFA and the n6 and n3 FA ratio were lower in the counseling group (p ¼ 0.043 and p ¼ 0.029, respectively). There were no differences between the groups in TAG FA in 1-month samples (Table 2). The group differences were not significant in CE FA in either time point (Table 3). The impact of dietary counseling on concentrations (mg/ L) of serum FA The concentration of eicosapentaenoic acid (20:5n3, EPA) in TAG (Table 4) was statistically significantly increased from cord blood to 1-month in children whose mothers received dietary counseling, but declined in control subjects (time group interaction p ¼ 0.009; rmANOVA). When evaluating the two time points separately, the dietary counseling had no effect on FA concentrations in cord blood or 1-month in TAG (Table 4) or CE (Table 5) fractions.
Discussion Maternal dietary counseling ensuing heightened intakes of PUFA and lowered intakes of SFA was reflected in FA composition of cord serum as an increased proportion of n3 FA and reduced proportion of SFA in TAG fraction. Our findings confirm the delivery of maternal dietary changes during pregnancy to the infant, the TAG FA representing a biomarker of exposure to exogenous FA over a very recent period of dietary intake (Lagstro¨m et al., 1998). The modification of infant’s FA status at an early stage may be of importance and carry long-term health benefits up to adulthood (Barman et al., 2013; Kaikkonen et al., 2012).
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Int J Food Sci Nutr, 2014; 65(3): 268–272
Table 2. Serum triacylglycerol fatty acids as proportion (%) of the total fatty acids from cord and 1-month samples in the intervention and the control groupsa. Cord blood
1-month
Intervention (n ¼ 31) Control (n ¼ 28) Mean Mean SD Mean SD difference Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n 3 22:6n3b Sum n3 n6/n3
34.91 2.27 41.52 3.62 23.58 3.95 9.89 1.79 0.49 0.13 0.83 0.16 3.49 0.99 0.60 0.17 0.86 0.26 16.16 2.60 0.65 0.22 0.85 0.45 0.60 0.32 1.47 0.50 6.53 2.45 2.72 0.81
36.22 2.61 42.02 3.28 21.76 3.53 9.59 2.34 0.50 0.18 0.85 0.31 3.22 0.88 0.57 0.14 0.85 0.30 15.58 2.93 0.62 0.23 0.78 0.34 0.47 0.18 1.29 0.37 5.08 1.32 3.22 0.91
1.31 0.50 1.81 0.30 0.01 0.02 0.27 0.03 0.01 0.58 0.03 0.06 0.13 0.18 1.46 0.50
95% CI 2.59, 2.31, 0.15, 0.78, 0.09, 0.15, 0.22, 0.05, 0.13, 0.86, 0.09, 0.15, 0.00, 0.05, 0.44, 0.95,
0.04* 1.31 3.78 1.38 0.07 0.11 0.76 0.12 0.16 2.02 0.15 0.27 0.26 0.41 2.48* 0.06*
Intervention (n ¼ 33) Control (n ¼ 31) Mean Mean SD Mean SD difference 35.42 4.25 47.19 2.69 17.39 2.38 12.40 2.27 0.17 0.10 0.35 0.11 0.94 0.32 0.12 0.05 0.08 0.06 14.06 2.10 1.67 0.47 0.29 0.20 0.26 0.14 0.78 0.45 3.01 1.02 5.29 2.33
36.10 3.26 46.97 3.26 16.93 2.97 12.09 2.72 0.17 0.11 0.36 0.12 0.94 0.31 0.14 0.07 0.10 0.10 13.79 2.82 1.48 0.44 0.25 0.23 0.26 0.11 0.76 0.47 2.75 0.83 5.44 1.90
0.68 0.22 0.46 0.31 0.00 0.01 0.01 0.01 0.02 0.27 0.19 0.04 0.00 0.02 0.26 0.15
95% CI 2.58, 1.27, 0.88, 0.94, 0.06, 0.07, 0.15, 0.04, 0.06, 0.97, 0.04, 0.07, 0.06, 0.21, 0.21, 1.22,
1.22 1.71 1.80 1.56 0.05 0.05 0.16 0.02 0.02 1.50 0.42 0.15 0.07 0.25 0.73 0.91
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses. *p50.05.
b
Table 3. Serum cholesterol ester fatty acids as proportion (%) of the total fatty acids from cord and 1-month samples in the intervention and the control groupsa. Cord blood
Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n 6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n3 22:6n3b Sum n3 n6/n3
1 month
Intervention (n ¼ 31) Mean SD
Control (n ¼ 28) Mean SD
Mean difference
24.0 2.0 42.3 4.7 33.7 4.8 16.2 2.0 0.72 0.24 1.45 0.23 12.1 2.8 0.01 0.03 0.15 0.17 30.6 4.4 0.28 0.18 0.85 0.40 0.04 0.12 1.47 0.50 2.65 0.8 12.4 3.1
24.2 1.2 42.1 4.0 33.7 4.2 16.3 2.8 0.78 0.23 1.48 0.43 12.0 2.2 0.02 0.1 0.11 0.13 30.6 4.2 0.28 0.16 0.80 0.31 0.01 0.04 1.29 0.37 2.38 0.7 13.7 3.8
0.21 0.21 0.00 0.10 0.06 0.02 0.13 0.01 0.03 0.03 0.00 0.06 0.03 0.18 0.26 1.36
95% CI 1.05, 2.08, 2.34, 1.38, 0.18, 0.20, 1.20, 0.05, 0.05, 2.25, 0.09, 0.13, 0.02, 0.05, 0.14, 3.18,
0.63 2.49 2.35 1.18 0.06 0.16 1.47 0.03 0.11 2.20 0.09 0.25 0.08 0.41 0.67 0.46
Intervention (n ¼ 33) Mean SD
Control (n ¼ 31) Mean SD
Mean difference
19.0 2.0 34.2 2.9 46.8 3.5 36.7 3.6 0.45 0.11 0.78 0.17 6.32 1.73 0.00 0.01 0.09 0.10 44.3 3.5 0.66 0.20 0.70 0.41 0.03 0.03 0.70 0.23 2.08 0.73 24.4 10.6
19.4 1.7 34.6 3.5 46.0 4.2 36.0 3.9 0.48 0.16 0.80 0.16 6.25 1.61 0.00 0.01 0.08 0.09 43.6 4.3 0.58 0.17 0.68 0.35 0.02 0.04 0.70 0.21 1.98 0.50 23.5 6.5
0.39 0.39 0.79 0.68 0.02 0.02 0.07 0.00 0.01 0.72 0.08 0.02 0.01 0.00 0.10 0.91
95% CI 1.32, 2.01, 1.13, 1.19, 0.09, 0.11, 0.77, 0.01, 0.04, 1.22, 0.02, 0.17, 0.01, 0.10, 0.21, 3.53,
0.54 1.23 2.71 2.55 0.05 0.06 0.91 0.01 0.06 2.66 0.17 0.21 0.02 0.11 0.42 5.34
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses.
b
Dietary counseling, an approach applicable to public health setting, resulted in increased intakes of n3 FA in the intervention group over the entire course of pregnancy and lactation, also reported previously in the larger study population (Ilmonen et al., 2011; Piirainen et al., 2006) Continuous supply of FA from the usual diet was ensured through supporting dietary counseling with provision of rapeseed oil based food products from early pregnancy onwards. This approach was evaluated feasible to induce health-benefits in both mother and child, as women of childbearing age possess a capacity for ALA conversion to longer chain derivatives like DHA and EPA (Burdge & Wootton, 2002). Further, we have previously demonstrated the impact of maternal dietary counseling in improving markers of essential FA and functional DHA status in cord blood PL FA (Niinivirta et al., 2011). Thus, we expected to demonstrate changes also in the lipid
fractions reflecting shorter-term dietary intake, namely, in TAG and CE fractions. In previous studies both TAG and CE FA have been successfully used as biomarkers for dietary intake in adults (Baylin & Campos, 2006) and children (Lagstro¨m et al., 1998; Moilanen et al., 1983; Nikkari et al., 1983), but to our knowledge there is no data on the impact of maternal dietary modification on infant TAG and CE FA. Previous intervention studies during pregnancy have usually analyzed PL FA as markers for dietary FA intake (de Groot et al., 2004; Helland et al., 2001, 2006; KraussEtschmann et al., 2007). While PL FA represent a time period of weeks to months, CE are considered to reflect consumption from a few days to 1–2 weeks and TAG from the last few days (Hodson et al., 2008; Zock et al., 1997). Our results suggest that TAG FA might be used as markers of infant FA supply through maternal diet during pregnancy.
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Table 4. Serum triacylglycerol fatty acids as concentration (mg/L) from cord and 1-month samples in the intervention and the control groupsa. Cord blood
Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n3 22:6n3b Sum n3
1-month
Intervention (n ¼ 31) Mean SD
Control (n ¼ 28) Mean SD
Mean difference
9.10 4.87 10.79 5.68 6.29 3.73 2.69 1.69 0.13 0.08 0.22 0.13 0.95 0.68 0.17 0.13 0.23 0.16 4.38 2.76 0.18 0.12 0.20 0.12 0.17 0.13 1.13 0.71 1.68 1.02
12.22 11.47 13.98 12.69 7.50 7.14 3.52 3.83 0.16 0.16 0.30 0.36 1.04 0.95 0.20 0.20 0.29 0.29 5.50 5.61 0.22 0.22 0.23 0.15 0.17 0.17 1.03 0.83 1.65 1.33
3.12 3.18 1.21 0.83 0.03 0.08 0.10 0.03 0.05 1.12 0.05 0.02 0.01 0.10 0.03
95% CI 7.87, 8.47, 4.26, 2.42, 0.10, 0.23, 0.52, 0.12, 0.18, 3.49, 0.14, 0.09, 0.09, 0.30, 0.59,
1.62 2.10 1.83 0.76 0.04 0.07 0.33 0.05 0.07 1.25 0.05 0.05 0.07 0.51 0.64
Intervention (n ¼ 33) Mean SD
Control (n ¼ 31) Mean SD
Mean difference
34.25 16.57 45.75 21.80 16.85 8.65 12.24 6.74 0.14 0.06 0.32 0.17 0.85 0.43 0.11 0.06 0.07 0.05 13.73 7.21 1.64 1.01 0.24 0.17 0.24 0.17 0.70 0.53 2.81 1.67
32.73 13.88 42.28 16.48 15.29 6.51 11.06 5.11 0.14 0.06 0.31 0.15 0.81 0.35 0.12 0.07 0.09 0.09 12.54 5.57 1.38 0.71 0.17 0.10 0.22 0.10 0.62 0.37 2.39 1.05
1.52 3.47 1.56 1.18 0.00 0.01 0.04 0.01 0.02 1.19 0.26 0.06 0.02 0.08 0.42
95% CI 6.14, 6.23, 2.28, 1.82, 0.03, 0.07, 0.16, 0.04, 0.06, 2.04, 0.18, 0.00, 0.05, 0.15, 0.28,
9.18 13.18 5.41 4.18 0.03 0.09 0.23 0.02 0.01 4.43 0.70 0.13 0.09 0.31 1.12
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses.
b
Table 5. Serum cholesteryl ester fatty acids as concentration (mg/L) from cord and 1-month samples in the intervention and the control groupsa. Cord blood
Sfa Mufa Pufa 18:2n6 18:3n6 20:3n6 20:4n6 22:4n6 22:5n6 Sum n6 18:3n3 20:5n3 22:5n3 22:6n3b Sum n3
1-month
Intervention (n ¼ 31) Mean SD
Control (n ¼ 28) Mean SD
Mean difference
16.78 5.82 29.41 9.97 23.31 8.40 11.22 4.04 0.49 0.21 1.00 0.34 8.36 3.44 0.01 0.02 0.01 0.11 21.17 7.71 0.19 0.12 0.59 0.33 0.02 0.06 1.02 0.51 1.83 0.81
16.57 5.56 28.81 10.57 22.79 7.22 10.93 3.53 0.52 0.20 1.02 0.42 8.13 3.02 0.02 0.09 0.08 0.09 20.69 6.73 0.19 0.11 0.53 0.23 0.01 0.03 0.88 0.38 1.61 0.62
0.21 0.60 0.51 0.30 0.03 0.02 0.22 0.01 0.02 0.47 0.01 0.06 0.02 0.14 0.22
95% CI 2.77, 4.76, 3.59, 1.69, 0.14, 0.22, 1.47, 0.04, 0.03, 3.32, 0.05, 0.09, 0.01, 0.10, 0.16,
3.18 5.96 4.62 2.28 0.07 0.18 1.92 0.02 0.07 4.26 0.07 0.20 0.04 0.38 0.60
Intervention (n ¼ 33) Mean SD
Control (n ¼ 31) Mean SD
Mean difference
24.86 8.44 44.97 14.52 61.33 19.64 48.06 15.57 0.58 0.20 1.02 0.40 8.31 3.62 0.00 0.01 0.13 0.02 58.09 18.64 0.87 0.40 0.91 0.60 0.03 0.05 0.41 0.07 2.73 1.30
27.00 7.72 48.37 14.35 63.85 16.58 50.03 13.50 0.65 0.22 1.09 0.29 8.62 2.91 0.00 0.02 0.12 0.02 60.50 15.78 0.83 0.39 0.94 0.54 0.03 0.05 0.40 0.07 2.77 1.05
2.14 3.40 2.52 1.97 0.07 0.07 0.31 0.00 0.01 2.41 0.04 0.03 0.01 0.05 0.04
95% CI 6.19, 10.62, 11.63, 9.27, 0.17, 0.24, 1.94, 0.01, 0.06, 11.07, 0.16, 0.31, 0.02, 0.26, 0.63,
1.91 3.82 6.59 5.33 0.04 0.10 1.33 0.01 0.07 6.25 0.23 0.26 0.03 0.15 0.56
a
Data were analyzed by independent-samples t test. Eluted with 24:1 in the analyses.
b
Although the detected changes in cord blood TAG FA were as expected, no effect by the maternal dietary intervention in CE FA was observed. One apparent reason for the lack of effect is related to the magnitude of change in the dietary FA content achieved through counseling. Although the change was evident, it remained modest compared for example to a recent dietary intervention study providing fish (salmon) to expecting mothers (Miles et al., 2011). The change in blood lipid FA is clearly related to the dose of FA administered, as demonstrated by several studies using fish oil supplements (Brown et al., 1990; Harris et al., 1983). In a similar way, the effect ensuing to the infant has been demonstrated in previous intervention studies using FA supplements to the mother (Helland et al., 2006; Jensen et al., 2000; Krauss-Etschmann et al., 2007). In the present study, no changes were observed in FA status at 1 month of age, although maternal dietary changes as well as modification of breast milk FA composition following the dietary counseling was verified (Hoppu et al., 2012). In the breast milk of the mothers receiving counseling, the proportion of a-linolenic acid (ALA, 18:3n3)
and total n3 FA increased and the ratio of n6/n3 FA was decreased compared to the control women (Hoppu et al., 2012). This further supports the notion that more intense dietary changes are required to induce FA status modification of the infant, particularly during the post-natal period. Moreover, when interpreting the results, some biological aspects of FA metabolism during pregnancy and breastfeeding need to be taken in consideration. Firstly, dietary FA might be utilized by maternal metabolism: FA are incorporated into cell membranes in tissues and particularly long-chain PUFA act as substrates for synthesis of eicosanoids (Sala-Vila et al., 2008). This is relevant particularly during pregnancy and lactation, because the metabolic demand of FA is increased. Secondly, selective placental fatty acid transfer (biomagnification) during gestation (Haggarty, 2010) could level the possible differences between different dietary intakes at time of birth and thus between study groups. Further, modification of FA by dietary counseling is challenging in this population of well-nourished and welleducated women, who already present with relatively high
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proportions of unsaturated FA in the diet or in the body. Naturally, a larger sample size might be of help in demonstrating differences between the study groups in further studies.
Conclusions Our results suggest that cord blood TAG FA may be used as dietary markers of infant FA status reflecting a change in maternal diet. Early modification of infant’s FA status by increasing the proportion of unsaturated FA, particularly n3 FA, may be of importance both in the short (Kremmyda et al., 2011) and long term, benefits possibly extending up to adulthood (Barman et al., 2013; Kaikkonen et al., 2012). However, as no changes in the CE FA or FA at 1 month of age were detected, it may be speculated that more drastic measures, such as supplementation of FA, in either maternal or infant diet may be necessary.
Acknowledgements We would like to thank Ulla-Maija Eriksson for her clinical work with the study participants and Patrick Gallagher for the grammatical review of the article. Provision of food products was by Raisio plc (Raisio, Finland).
Declaration of interest This work was supported in part by a grant from the Social Insurance Institution of Finland, the Academy of Finland, the Yrjo¨ Jahnsson Foundation and a personal grant from the Maud Kuistila Memorial Foundation for KN. The authors declare no conflicts of interests. The authors alone are responsible for the content and writing of this article.
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