Applied nutritional investigationFatty acid status and antioxidant defense system in mothers and their newborns after salmon intake during late pregnancy
Introduction
The requirements for the long-chain polyunsaturated fatty acids (LC-PUFA) arachidonic acid (AA, C20:4 ω-6) and docosahexaenoic acid (DHA, C22:6 ω-3) are especially high during the last trimester of pregnancy and the first weeks of extrauterine life because of their accretion into the growing brain and other tissues [1], [2]. AA and DHA can be formed by elongation and desaturation of the essential precursors linoleic acid (LA; C18:2 ω-6) and α-linolenic acid (ALA; C18:3 ω-3), respectively, but fetal fatty acid-desaturase enzymes are unable to supply sufficient LC-PUFA until 16 wk after birth [3]. Therefore, fetal LC-PUFA must be supplied from the maternal circulation and so are ultimately derived from the maternal diet.
The increased fetal demand for LC-PUFA is indicated by a concomitant decrease in the relative concentrations of DHA and AA in the maternal plasma as pregnancy progresses [4], [5]. Fish oils rich in ω-3 LC-PUFA, DHA and eicosapentaenoic acid (EPA; 20:5 ω-3), may enhance maternal, fetal, and neonatal PUFA status. Findings from several studies have shown that dietary intakes of ω-3 LC-PUFA of ≥2.6 g/d significantly increase the ω-3 LC-PUFA status in both pregnant women and their newborns [6], [7], [8]. Nonetheless, this increase may be accompanied by a reduction of ω-6 LC-PUFA toward the end of pregnancy [8], [9], [10], [11], and this is not desirable.
The UK government recommends that pregnant women consume one or two portions of oily fish each week as a source of ω-3 LC-PUFA [10]. It is not clear whether consumption of fish as a whole food delivering ω-3 LC-PUFA affects the ω-3 LC-PUFA status of mothers and their newborns. In this regard, one study observed higher EPA and DHA status and lower AA status in mothers with high dietary intake of oily fish in relation to those with lower consumption, with similar findings in newborns [11]. To our knowledge, no intervention studies apart from Salmon in Pregnancy Study (SiPS) [12] have investigated the effect of higher oily fish intake in pregnant women whose consumption of oily fish was normally low. In SiPS, the intake of two portions of salmon per week (equivalent to a daily intake of about 500 mg EPA + DHA) resulted in an enhanced plasma EPA and DHA status in pregnant women, and a higher EPA and DHA status in the umbilical cord blood plasma than seen in the control group [12].
It is known that LC-PUFAs are good substrates for lipid peroxidation, and so a diet high in ω-3 LC-PUFA could contribute to oxidative stress [13]. However, several mechanisms exist to protect against peroxidative damage. These mechanisms involve exogenous vitamins and trace elements as well as endogenous enzyme systems [14]. In SiPS, maternal oxidative stress markers remained unaffected after consumption of two portions of salmon per week [15]. Furthermore, maternal retinol and selenium (Se) levels were significantly higher in the group supplemented with salmon than in the control group [16]. To our knowledge, there are no studies on the effect of increased maternal oily fish intake on the antioxidant defense system in newborns.
Therefore, the aims of the present study, as part of SiPS, were to examine the effect of increased salmon consumption beginning in week 20 of pregnancy through delivery (1) on erythrocyte fatty acids in pregnant women and their newborns and (2) on the antioxidant defense system in the newborns' blood.
Section snippets
Materials and methods
The study design, characteristics of the pregnant women, aspects of their diet, and compliance have been described in detail elsewhere [12]. In brief, 123 pregnant women residing in or near Southampton, United Kingdom were enrolled in the study. The inclusion criteria were age 18 to 40 y; <19 wk gestation; healthy, uncomplicated, singleton pregnancy; having a baby at risk for atopy; consuming less than two portions of oily fish per month, excluding tinned tuna; and not taking fish oil
Results
As reported previously [12], the two groups did not differ in maternal age, height, or weight, or in infant birth weights or skin prick test positivity. Additionally, the percentages of EPA and DHA in plasma phospholipids decreased during pregnancy in the control group [12]. This decline did not occur in the salmon group; indeed, the percentages of EPA and DHA increased so that both were higher in the salmon group than in the control group at weeks 34 and 38 [12].
Discussion
In normal pregnancies, there is a physiological insulin resistance during the last trimester that promotes maternal lipolysis, to ensure the provision of fatty acids to the fetus [26]. Among these fatty acids, ω-3 LC-PUFA are the most important because they are essential for normal fetal brain development [1] and for visual acuity [2]. Additionally, adequate levels of ω-6 LC-PUFA are necessary during early development [27], [28]. In the present study, erythrocyte AA proportions increased during
Conclusions
Limited attention has been given to the antioxidant defense system of the fetus in relation to maternal LC-PUFA exposure and, probably never before, when the source of ω-3 LC PUFA is oily fish. The present study demonstrated that the consumption of farmed salmon twice a week from week 20 of pregnancy until delivery (providing about 500 mg/wk of EPA + DHA) did not impair the antioxidant defense system and did not alter erythrocyte fatty acid composition in newborns or their mothers.
Acknowledgments
The authors acknowledge the staff and volunteers who assisted with this study.
References (39)
- et al.
Intrauterine fatty acid accretion rates in human brain: Implications for fatty acid requirements
Early Hum Dev
(1980) Tissue levels of polyunsaturated fatty acids during early human development
J Pediatr
(1992)- et al.
Are long-chain polyunsaturated fatty acids essential nutrients in infancy?
Lancet
(1995) - et al.
The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes
Int J Biochem Cell Biol
(2010) - et al.
Direct transesterification of all classes of lipids in a one-step reaction
J Lipid Res
(1986) Catalase in vitro
Methods Enzymol
(1984)- et al.
Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein)
J Biol Chem
(1969) - et al.
High-performance liquid chromatography-EC assay of mitochondrial coenzyme Q9, coenzyme Q9 H2, coenzyme Q10, coenzyme Q10 H2, and vitamin E with a simplified on-line solid phase extraction
Methods Enzymol
(2004) - et al.
Quantitation of reduced and total glutathione at the femtomole level by high-performance liquid chromatography with fluorescence detection: application to red blood cells and cultured fibroblasts
J Chromatogr B Biomed Sci Appl
(2001) Placental delivery of arachidonic and docosahexaenoic acids: implications for the lipid nutrition of preterm infants
Am J Clin Nutr
(2000)
Infant plasma trans, n-6, and n-3 fatty acids and conjugated linoleic acids are related to maternal plasma fatty acids, length of gestation, and birth weight and length
Am J Clin Nutr
Effect of three low-dose fish oil supplements, administered during pregnancy, on neonatal long-chain polyunsaturated fatty acid status at birth
Prostaglandins Leukot Essent Fatty Acids
Docosahexaenoic acid supply in pregnancy affects placental expression of fatty acid transport proteins
Am J Clin Nutr
Long-chain polyunsaturated fatty acid (LC-PUFA) transfer across the placenta
Clin Nutr
Plasma tocopherol levels and vitamin E/beta-lipoprotein relationships during pregnancy and in cord blood
Am J Clin Nutr
Red blood cell vitamin E concentrations in fetuses are related to but lower than those in mothers during gestation. A possible association with maternal lipoprotein plasma levels
Am J Obstet Gynecol
Biochemical EFA status of mothers and their neonates after normal pregnancy
Early Hum Dev
Intake of long chain ω-3 polyunsaturated fatty acids during pregnancy and the influence of levels in the mother on newborn levels
Eur J Obstet Gynecol Reprod Biol
Maternal essential fatty acid patterns during normal pregnancy and their relationship to the neonatal essential fatty acid status
Br J Nutr
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This study was supported by the European Commission under Framework 6: Sustainable aqua feeds to maximize the health benefits of farmed fish for consumers (AQUAMAX; FOOD-CT-2006-16249). PCC, EAM, and KMG designed the Salmon in Pregnancy Study and PCC had overall responsibility for all aspects of the study. AG had overall responsibility for the work related to the present article. MV, L-SK, NDD, and PSN conducted research. MDM and CMA monitored the data. CEG-R analyzed the data. CEG-R and JO drafted the manuscript. JO, MDM, PCC, and AG had significant input into the manuscript. All authors have read and approved the final manuscript. KMG and PCC are supported by the National Institute for Health Research through the NIHR Southampton Biomedical Research Centre; KMG is also supported by the European Union's Seventh Framework Programme (FP7/2007-2013), projects Early Nutrition and ODIN under grant agreements numbers 289346 and 613977. CEG-R is the recipient of a fellowship from the Spanish Ministry of Education. The authors have no conflicts of interest to declare.