Does consumption of two portions of salmon per week enhance the antioxidant defense system in pregnant women?
ABSTRACT Salmon is a rich source of marine n-3 fatty acids, which may increase oxidative stress and, in turn, could affect the antioxidant defense system in blood plasma and erythrocytes of pregnant women. The Salmon in Pregnancy Study provided two meals of salmon per week to pregnant women from week 20 of gestation; the control group maintained their habitual diet low in oily fish. Higher selenium and retinol plasma concentrations were observed after dietary salmon supplementation. Besides, a concomitant increase in selenium and glutathione concentration as well as glutathione peroxidase and reductase activities were detected as pregnancy progressed. However, tocopherols, retinol, β-carotene, and coenzyme Q(10) decreased in late pregnancy. Collectively, our findings lead to the hypothesis that increased farmed salmon intake may increase antioxidant defenses during pregnancy. Clinical trials identifier NCT00801502.
- [Show abstract] [Hide abstract]
ABSTRACT: Changes in paraoxonase 1 (PON1) activities have been observed in a variety of diseases involving oxidative stress, such as CVD. However, its role in obesity has not been fully established. In the present study, we aimed (1) to genotype sixteen PON1 SNP, (2) to measure serum PON1 activities and (3) to correlate these findings with the incidence of childhood obesity and related traits. We conducted a case-control study of 189 normal-weight and 179 obese prepubertal children, and we measured four different PON1 activities: lactonase; paraoxonase; arylesterase; diazoxonase. Although none of these activities was significantly different between the obese and normal-weight children, lactonase activity was found to be positively correlated with HDL-cholesterol and ApoA1 levels and negatively correlated with myeloperoxidase and fatty acid-binding protein 4 levels. Among the sixteen genotyped PON1 SNP, only the intronic SNP rs854566 exhibited a significant association with obesity (OR 0·61, 95 % CI 0·41, 0·91; P= 0·016). This genetic variant was also associated with increased diazoxonase, lactonase and arylesterase activities and decreased paraoxonase activity. Other genetic variants exhibited different association patterns with serum activities based on their location within the PON1 gene, and SNP that were located within the promoter were strongly associated with lactonase, arylesterase and diazoxonase activities. The functional variant Q192R exhibited the greatest effect on paraoxonase activity (P= 5·88 × 10- 42). In conclusion, SNP rs854566 was negatively associated with childhood obesity and with increased serum PON1 activities in prepubertal children. We determined that lactonase is a reliable indicator of PON1 activities and should be included in future studies of PON1 function.The British journal of nutrition 06/2013; · 3.45 Impact Factor
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ABSTRACT: In this study the effect of increasing dietary alpha tocopherol on vitamin E tissue concentrations, lipid peroxidation (malondialdehyde), antioxidant enzymes, and fatty acid composition has been investigated in farmed Atlantic salmon. To this end fish (initial body weight ~ 193 g, n = 70 per group) were fed diets based on fish oil (27.5 %), fish meal (15.0 %), wheat gluten (20.6 %), and soy protein concentrate (24.0 %) for 14 weeks. Diets were supplemented with 0 (negative control), 150, and 400 mg/kg vitamin E as all-rac alpha-tocopheryl acetate. Dietary vitamin E did not affect feed conversion efficiency ratio but significantly (p < 0.05) increased alpha-tocopherol concentrations in salmon plasma, liver, and fillet (n = 8 per group each). The increase in fillet alpha-tocopherol was accompanied by a considerable decrease (p < 0.01) in malondialdehyde concentrations at the higher supplementation level. Furthermore, we observed an antagonistic interaction between alpha- and gamma-tocopherol in plasma at the highest supplementation level, since high dietary alpha-tocopherol reduced plasma gamma-tocopherol concentrations. Liver antioxidant enzymes, including glutathione peroxidase and superoxide dismutase, remained largely unchanged in response to dietary alpha-tocopherol. Dietary alpha-tocopherol did not affect eicosapentaenoic acid and docosahexaenoic acid concentrations in salmon fillet. Present data suggest that alpha-tocopherol supplementations beyond dietary recommendations may further improve flesh quality and nutritional value of Atlantic salmon fillet as far as malondialdehyde and vitamin E concentrations are concerned.International Journal for Vitamin and Nutrition Research 08/2013; 83(4):238-45. · 1.00 Impact Factor
NEWS & VIEWS
Does Consumption of Two Portions of Salmon Per Week
Enhance the Antioxidant Defense System
in Pregnant Women?
Cruz E. Garcı ´a-Rodrı ´guez,1Marı ´a D. Mesa,1Josune Olza,1Maria Vlachava,2Lefkothea-Stella Kremmyda,2
Norma D. Diaper,2Paul S. Noakes,2Elizabeth A. Miles,2Marı ´a Carmen Ramı ´rez-Tortosa,1
Bjørn Liaset,3Livar Frøyland,3Adrien Rossary,4Marie-Chantal Farges,4Marie-Paule Vasson,4,5
Concepcion M. Aguilera,1Johanna Helmersson-Karlqvist,6–8Keith M. Godfrey,2,9, 10
Philip C. Calder,2, 10Samar Basu,4,6,7and A´ngel Gil1
Salmon is a rich source of marine n-3 fatty acids, which may increase oxidative stress and, in turn, could affect
the antioxidant defense system in blood plasma and erythrocytes of pregnant women. The Salmon in Pregnancy
Study provided two meals of salmon per week to pregnant women from week 20 of gestation; the control group
maintained their habitual diet low in oily fish. Higher selenium and retinol plasma concentrations were observed
after dietary salmon supplementation. Besides, a concomitant increase in selenium and glutathione concentra-
tion as well as glutathione peroxidase and reductase activities were detected as pregnancy progressed. However,
tocopherols, retinol, b-carotene, and coenzyme Q10decreased in late pregnancy. Collectively, our findings lead
to the hypothesis that increased farmed salmon intake may increase antioxidant defenses during pregnancy.
Clinical trials identifier NCT00801502. Antioxid. Redox Signal. 16, 1401–1406.
present during oxidative stress as a consequence of an im-
balance between the formation and inactivation of these
species. The antioxidant defense system (ADS) provides
protection to avoid ROS-induced damage of cellular compo-
nents. The capacity of this defense system is determined by a
dynamic interaction between individual components, which
include vitaminsA, E, and b-carotene, coenzyme Q10(CoQ10),
glutathione, and several antioxidant enzymes. The most im-
portant enzymatic antioxidants are superoxide dismutase
(SOD), catalase (CAT), glutathione reductase (GR), and glu-
eactive oxygen species (ROS) are generated during
normal aerobic metabolism and increased levels are
tathione peroxidase (GPx), with selenium as part of several
selenium-proteins such as GPx.
Normal pregnancy is accompanied by a high metabolic
demand and elevated requirements for tissue oxygen, which
Marine n-3 fatty acidsmayincrease oxidative stress.The
Salmon in Pregnancy Study provided two meals of salmon
per week to pregnant women from week 20 of gestation
until parturition. An increase in antioxidant defenses was
observed compared with a control group of pregnant
women consuming their habitual diet.
1Department of Biochemistry and Molecular Biology II, Biomedical Research Center, Institute of Nutrition and Food Technology ‘‘Jose ´
Mataix,’’ University of Granada, Granada, Spain.
2Developmental Origins of Health and Disease Division, School of Medicine, University of Southampton, Southampton, United Kingdom.
3National Institute of Nutrition and Seafood Research, Bergen, Norway.
4EA 4233, University d’Auvergne, Clermont University, CRNH Auvergne, CLARA, Clermont-Ferrand, France.
5Clinical Nutrition Department, Anticancer Institute Jean-Perrin, Clermont-Ferrand, France.
6Oxidative Stress and Inflammation, Department of Public Health and Caring Sciences, Faculty of Medicine, Uppsala University, Uppsala,
7Centre of Excellence-Inflammation, Uppsala University Hospital, Uppsala, Sweden.
8Clinical Chemistry, Department of Medical Sciences, Uppsala University Hospital, Uppsala, Sweden.
9Southampton Medical Research Council Lifecourse Epidemiology Unit, University of Southampton, Southampton, United Kingdom.
10Southampton NIHR Nutrition, Diet and Lifestyle Biomedical Research Unit, Southampton University Hospitals NHS Trust, South-
ampton, United Kingdom.
ANTIOXIDANTS & REDOX SIGNALING
Volume 16, Number 12, 2012
ª Mary Ann Liebert, Inc.
results in increased oxidative stress (8). If oxidative stress is a
risk of pregnancy, then the mother’s diet (specifically, the
intakes of antioxidants, polyunsaturated fatty acids, and
other unknown beneficial radical scavenging compounds)
may play a role in modifying that process. The Salmon in
Pregnancy Study (SiPS) isthe first intervention trial withoily
fish, rich in n-3 long chain-polyunsaturated fatty acids (n-3
LCPUFA), during pregnancy, and focuses on pregnant wo-
men whose offspring are at high risk of developing atopic
diseases (6). Epidemiological data suggest that early expo-
sure to oily fish (e.g., during pregnancy or infancy) is asso-
ciated with lower risk of atopy and allergic disorders in
children (5). However, LCPUFAs are susceptible to perox-
idation due to their high degree of unsaturation. Therefore,
increased dietary consumption of n-3 LCPUFA might en-
hance oxidative stress with potential untoward effects dur-
ing pregnancy. Thus, the hypothesis of the present study
was that the consumption of two portions of salmon per
week during gestation would increase oxidative stress and,
in turn,would affect the ADS. Nonetheless, we have recently
reported that increased salmon intake did not result into an
increased oxidative stress in the same study popula-
tion (by measurement of F2-isoprostanes, 8-hydroxy-2¢-
deoxyguanosine, and lipid hydroperoxides) (4).
Indeed, the aim of this work, part of the SiPS, was to
and without increased salmon consumption from week 20 of
pregnancy. Particularly, we compared the concentration of
plasma tocopherols, retinol, b-carotene, and CoQ10, as well
as glutathione and selenium, along with the activities of the
key antioxidant enzymes CAT, SOD, GR, and GPx in
Salmon Intake and Its Consequences for the ADS
Asreportedpreviously (6), the twogroups did not differ in
age, height, weight, or birth weight of offspring or with re-
spect to skin prick test positivity (Supplementary Table S1;
.liebertonline.com/ars). Further, pregnant women from SiPS
increased their intakes of n-3 LCPUFA, enhanced their status
of eicosapentaenoic acid (EPA) and docosahexaenoic acid
(DHA), and increased the status of EPA and DHA in their
fetuses and neonates, after intake of two portions of salmon
per week (6).
Erythrocyte antioxidant enzymatic activities and selenium
and glutathione levels in pregnant women are shown in
Table 1. Erythrocyte SOD, CAT, and GR activities did not
differ between groups. However, GPx activity was signifi-
cantly higher in the salmon group than in the control group
(p=0.042). Values in the salmon group were higher but not
significantly different (p=0.409, p=0.087, and p=0.176, at
weeks 20, 34, and 38, respectively). When erythrocyte GPx
activity at baseline (i.e., week 20) was used as a covariate, GPx
activity tended to be higher in the salmon group (p=0.063).
Unlike other dietary factors, intakes of oily fish and indeed of
n-3 LCPUFA were by chance slightly, but significantly, dif-
ferent between groups at baseline (6). Erythrocyte selenium
concentration was significantly higher in the salmon group
than in the control group (p<0.001). Comparison between
groups at 20, 34, and 38 weeks of gestation showed significant
differences for selenium, with values in the salmon group
being higher (p=0.042, p<0.001, and p=0.018, respectively).
When week 20 selenium concentration was used as a covari-
ate, significant differences between groups were retained
(p=0.001). Erythrocyte glutathione (reduce, oxidized, and
total) concentrations were similar between groups. Ery-
throcyte GPx and GR activities along with selenium and
glutathione (reduced, oxidized, and total) concentrations in-
creased significantly during pregnancy (p ranging between
<0.001 and 0.029), while SOD and CAT activities did not
Plasma retinol, a- and c-tocopherol, b-carotene, and CoQ10
levels in pregnant women are shown in Table 2. Plasma
Table 1. Erythrocyte Antioxidant Enzymatic Activities and Selenium and Glutathione Levels in Pregnant
Women Consuming Their Habitual Diet (Control) or Consuming Salmon Twice Per Week (Salmon)
Control (n=54)Salmon (n=54)Source of variation
20 weeks34 weeks38 weeks20 weeks34 weeks38 weeks
CAT (nmol/L$g Hb) 2.96–0.14
SOD (U/mg Hb)
GR (U/g Hb)
GPx (U/g Hb)
Values are expressed as mean–standard error of mean.
*Statistically significant differences (p<0.05) between groups using a general linear model of variance. When GPx activity and selenium
concentration at week 20 were used as a covariate, significant differences between groups were seen only for selenium (p=0.001). Different
letters denote statistical differences between time points within the study groups (p<0.05).
CAT, catalase; GPx, glutathione peroxidase; GR, glutathione reductase; GSH, reduced glutathione; GSSG, oxidized glutathione; RBC, red
blood cell; SOD, superoxide dismutase.
1402GARCI´A-RODRI´GUEZ ET AL.
Table 2. Plasma Retinol, a- and c-Tocopherol, b-Carotene, and Coenzyme Q10Levels in Pregnant Women
Consuming Their Habitual Diet (Control) or Consuming Salmon Twice Per Week (Salmon)
Source of variation
a-tocopherol/total lipids (ng/mg)
c-tocopherol/total lipids (ng/mg)
b-carotene/total lipids (ng/mg)
Retinol/total lipids (ng/mg)
CoQ10/total lipids (ng/mg)
CoQ10H2/total lipids (ng/mg)
Total CoQ10/total lipids (ng/mg)
Values are expressed as mean–standard error of mean.
*Statistically significant differences (p<0.05) between groups using a general linear model of variance. When retinol at week 20 was used as a covariate, significant differences were retained (p=0.008).
Different letters denote statistical differences between time points within the study groups (p<0.05).
CoQ10, coenzyme Q10; CoQ10H2, reduced coenzyme Q10.
retinol was significantly higher in the salmon group than in
the control group (p=0.002). Significant differences were
found between groups at weeks 34 and 38 for retinol, with
higher values in the salmon group (p=0.032 and 0.003, re-
spectively). Significant differences between groups were re-
tained when week 20 retinol was used as a covariate
(p=0.008). None of the other nonenzymatic antioxidants an-
alyzed differed significantly between groups. During preg-
nancy, a- and c-tocopherol, retinol, b-carotene, and CoQ10
(oxidized, reduced, and total) decreased significantly (p
ranging from 0.002 to <0.001).
No interactions were seen for any of the parameters
determined when group and time effects were analyzed
Erythrocyte SOD, CAT, GR, and GPx activities, together
with glutathione concentrations, remained similar after
salmon supplementation, although activation of these
protective systems may occur by LCPUFAs (1). A differ-
ence in selenium concentration was seen between groups
at baseline, because oily fish intake was by chance slightly,
but significantly, different between groups at week 20 (6).
However, we also found significantly higher erythrocyte
selenium concentrations in the salmon group in mid-
pregnancy, reflecting an effect of salmon intake on sele-
nium concentration. This elevated selenium plasma level
might be an underlying factor to the increase observed for
GPx activity in the salmon group, despite not being sig-
nificant. Dietary selenium intake or supplementation has
been related to higher antioxidant enzymatic activity and
lower lipid peroxidation. In contrast, selenium deficiency
leads to a decline in tissue levels of selenium-dependent
antioxidant enzymes and thereby oxidative stress condi-
tions develop (9). Several authors have indicated that
supplementation with n-3 LCPUFA enhanced oxidative
stress at dietary intakes higher than that contained in the
fish supplied in our study (the equivalent of about
500mg/day). In this way, Filaire et al. (3) observed that n-3
however, it decreased when antioxidants were added in
combination with n-3 LCPUFAs. In fact, as mentioned
earlier, we did not find increased oxidative stress in our
study population after salmon supplementation (4). To-
gether with n-3 LCPUFA, oily fish supplies antioxidants,
which may prevent increased oxidative stress after in-
creased fish intake in pregnant women. In the present
study, plasma vitamin E levels were similar in both control
and salmon-supplemented groups. Since vegetable oils are
the main source of vitamin E, the quantity of this vitamin
provided by fish was relatively small. A similar behavior
to vitamin E was found for b-carotene, without differences
between groups. Beta-carotene is the precursor of retinol,
essentially important for growth and development of cells
and tissues. Plasma retinol concentration was significantly
higher in the salmon group than in the control group de-
spite that retinol concentration was also different between
groups at baseline (6). The higher retinol plasma concen-
tration in the salmon-supplemented group might be ex-
plained as a consequence of intake of salmon, since this
fish is known to be rich in retinol. CoQ10levels were not
affected by salmon intake. Therefore, n-3 LCPUFA may
have both pro-oxidant and antioxidant properties de-
pending on experimental conditions, dosage, and the an-
Another important finding of this study was that erythro-
cyte GPx and GR activities along with glutathione and sele-
nium concentration increased significantly in mid and late
pregnancy. Besides, SOD and CAT activities were not differ-
ent across the three time points studied. Information con-
cerning the changes of these enzymes during normal
pregnancy is conflicting and scarce. According to our results,
it seems that GPx and GR enzymes have a major role in the
elimination of blood peroxides generated during pregnancy.
The enhanced maternal components of the ADS observed in
our study population suggest a response of the antioxidant
defenses to pregnancy-induced increases in oxidative stress
(8). Our results also showed a significant decrease in all
plasma nonenzymatic antioxidant concentrations beyond
week 20 of pregnancy. This decline has been reported by
others (7) and might be an indication of a higher level of ox-
idative stress toward the end of gestation as well as the in-
creased maternal blood volume. The role of retinol and its
metabolites in reproduction and embryonic development
have been clearly established (2), and low cord and maternal
serum retinol have been associated with poor vitamin A sta-
tus, which in turn may affect fetal growth. The decline in
plasma retinol levels during late pregnancy may reflect its
enhanced transfer to and utilization by the fetus. Preservation
of fetal retinol levels at the expense of a decline on the ma-
ternal side is of pivotal importance for appropriate pregnancy
outcome and increased consumption of salmon could con-
tribute to it.
contentsofthe backgrounddiet andof
Concluding Remarks and Future Directions
Under the conditions of the SiPS, our findings lead to the
conclusion that increased consumption of salmon may raise
selenium and retinol concentrations in pregnant women,
with a concomitant increase in GPx and GR activities and
selenium and glutathione concentrations, throughout preg-
nancy. This elevation in antioxidant defenses might be
helpful to prevent and/or reduce additional oxidant stress
during pregnancy. However, the influence of n-3 LCPUFA
supplementation is still controversial and further research is
needed to explore how fish and their n-3 PUFAs may affect
Subjects and methodology
acteristics, aspects of their diet, and their compliance have
been described in detail elsewhere (6) (Supplementary Table
S1). The SiPS is a single-blind, randomized, controlled trial of
increased consumption of farmed salmon by pregnant wo-
men from week 20 of gestation until the end of their preg-
nancy. Supplementary Figure S1 shows the progress of
women through the study. In brief, a total of 123 pregnant
women in the area of Princess Anne Hospital (Southampton,
United Kingdom) were enrolled in the study. Inclusion cri-
teria were age 18 to 40 years; <19 weeks of gestation; healthy
uncomplicated singleton pregnancy; baby at risk of atopy
(one or more first-degree relatives of the baby affected by
atopy, asthma, or allergy by self-report); consuming <2
The study design, the subjects, and their char-
1404GARCI´A-RODRI´GUEZ ET AL.
portions of oily fish per month excluding tinned tuna; and not
using fish oil supplements currently or in the previous 3
months. All procedures were approved by the Southampton
and South West Hampshire Research Ethics Committee (07/
Q1704/43). The study was conducted according to the prin-
ciples of the Declaration of Helsinki and all women gave
written informed consent. The SiPS is registered at www
signed to one of two groups; randomization was according
to a random number table. Women in the control group
(n=61) were asked to continue their habitual diet, and wo-
men in the salmon group (n=62) were asked to incorporate
two portions of farmed-salmon (150g/portion) into their
diet per week from study entry (week 20) until they gave
birth. Farmed salmon for use in the SiPS was raised using
dietary ingredients selected to contain low levels of con-
taminants. Each 150g salmon portion contained (on aver-
age) 30.5g protein, 16.4g fat, 0.57g EPA, 0.35g DPA, 1.16g
DHA, 3.56g total n-3 PUFA, 4.1mg a-tocopherol, 1.6mg c-
tocopherol, 6lg vitamin A, 14lg vitamin D3, and 43lg se-
lenium. Thus, two portions of salmon per week would typ-
selenium. Contaminants contributed <12.5% of the FAO/
WHO provisional tolerable weekly intake for dioxin and
dioxin-like polychlorinated biphenyls, <11.5% for arsenic,
<0.00000008% for cadmium, 0.0000025% for mercury, and
<0.00000002% for lead.
Fifteen subjects were not able to complete the study for
various reasons (delivery before appointment, cancelled
because of feeling tiredness, busy, or some sort of injury),
leaving a total of 54 subjects in the control group and 54
subjects in the salmon group. As reported previously (6),
the two groups did not differ in age, height, weight, or birth
weight of offspring or with respect to skin prick test posi-
tivity (Supplementary Table S1). No adverse events or
negative health effects were observed or reported during
Fasting maternal venous blood samples for the laboratory
analyses were collected at week 20 of gestation, before the
intervention started, at week 34 and at week 38. After cen-
trifugation, aliquots of plasma and washed erythrocytes were
frozen immediately and stored at -80?C until analyzed.
Women also completed a 100-item food frequency question-
naire covering food intake over the preceding 12 weeks.
Recruited women were randomly as-
Determination of enzymatic antioxidant activities.
throcyte CAT, SOD, and GR activities were assayed spectro-
photometrically and expressed as nmol/(L$g Hb), U/mg Hb,
and U/g Hb, respectively. Erythrocyte GPx activity was de-
termined spectrophotometrically by the coupled enzyme
procedure with tert-butyl hydroperoxide as substrate and is
expressed as U/g Hb. Hemoglobin concentration in the blood
samples was determined spectrophotometrically by the col-
orimetric cyanmethemoglobin method, using Sigma Diag-
Determination of nonenzymatic antioxidant concentra-
Plasma concentrations of a- and c-tocopherol, reti-
nol, and CoQ10were determined by high-pressure liquid
chromatography coupled to an electrochemical detector
(HPLC-EC), after extraction with 1-propanol. b-carotene
was also determined after extraction with 1-propanol in a
HPLC system attached to a multi-wavelength ultraviolet
detector set at 450nm. All compounds were identified by
predetermining the retention times of individual stan-
dards. As all of them are lipid soluble, concentrations are
given by ml of plasma and in relation to total plasma
Plasma triacylglycerols, phospholipids, and total choles-
terol were measured spectrophotometrically using commer-
cial enzymatic assay kits from Spinreact (Girona, Spain)
(Triglycerides, Ref. 1001311, Phospholipids, Ref. 1001140; Total
cholesterol, Ref. 1001091), according to the manufacturer’s
protocols, and the results were standardized using standard
solutions for triacylglycerols, phospholipids, and total cho-
Erythrocyte selenium was determined by inductively cou-
pled plasma mass spectrometry on an Agilent 7500 ICPMS.
Selenium (78Se) concentration in red blood cell samples was
calculated using an external standard calibration. Frozen red
blood cells (RBCs) were thawed, and aliquots of *0.5g were
weighed. Selenium is expressed as lg Se/kg RBC.
Erythrocyte glultathione content was measured by HPLC
with fluorescence detection at 420nm, and is expressed as
Results are given as mean–standard error of mean.
Conformity toa normaldistribution was examined using the
Kolmogorov-Smirnov test. It was calculated that a sample
size of 50 women per group would have 93% power with a
type I error of alpha <0.05. Differences for each variable
between treatment groups over time were evaluated using a
general linear model of variance for repeated measures. A
posteriori Bonferroni tests were performed to evaluate spe-
cific differences within groups between the considered ges-
tational periods. When initial values were different, the
statistical analyses were corrected using baseline values as a
covariant. Mean comparisons for GPx, selenium, and retinol
at each gestational period were determined by a posteriori
Bonferroni tests. All statistical analyses were performed
with the Statistical Package of Social Science (SPSS) 15.0
for Windows. p-values <0.05 were considered statistically
(A fully referenced methodology may be viewed as Sup-
plementary Data online.)
This study was supported by the European Union
Commission under Framework 6: Sustainable aquafeeds to
maximize the health benefits of farmed fish for consumers
(AQUAMAX; FOOD-CT-2006-16249), and the Swedish
Society of Medical Research. The authors thank the staff
and volunteers who assisted with this study. We gratefully
acknowledge the technical contribution from Maria Borja
and Laura Campan ˜a. Cruz E. Garcia-Rodriguez is the
recipient of a fellowship from the Spanish Ministry of
ANTIOXIDANT DEFENSE SYSTEM AND SALMON IN PREGNANCY1405
1. Arab K, Rossary A, Flourie F, Tourneur Y, and Steghens JP.
Docosahexaenoic acid enhances the antioxidant response of
human fibroblasts by upregulating gammaglutamyl-cysteinyl
ligase and glutathione reductase. Br J Nutr 95: 18–26, 2006.
2. Clagett-Dame M and DeLuca HF. The role of vitamin A in
mammalian reproduction and embryonic development. Annu
Rev Nutr 22: 347–381, 2002.
3. Filaire E, Massart A, Rouveix M, Portier H, Rosado F, and
Durand D. Effects of 6 weeks of n-3 fatty acids and antioxi-
dant mixture on lipid peroxidation at rest and postexercise.
Eur J Appl Physiol 111: 1829–1839, 2011.
4. Garcı ´a-Rodrı ´guez CE, Helmersson-Karlqvist J, Mesa MD,
Miles EA, Noakes PS, Vlachava M, Kremmyda S, Diaper ND,
Godfrey KM, Calder PC, Gil A, and Basu S. Does increased
intake of salmon increase markers of oxidative stress in
pregnant women?-The Salmon in Pregnancy Study. Antioxid
Redox Signal 15: 2819–2823, 2011.
5. Kremmyda LS, Vlachava M, Noakes PS, Diaper ND, Miles
EA, and Calder PC. Atopy risk in infants and children in
relation to early exposure to fish, oily fish, or long-chain
omega 3-fatty acids: a systematic review. Clin Rev Allergy
Immunol 41: 36–66, 2011.
6. Miles EA, Noakes P, Kremmyda L-S, Vlachava M, Diaper ND,
Rosenlund G, Urwin H, Yaqoob P, Rossary A, Farges M-C,
Vasson M-P, Liaset B, Froyland L, Helmersson J, Basu S,
Garcia E, Olza J, Mesa MD, Aguilera CM, Gil A, and Calder
PC. The salmon in pregnancy study- study design, subject
characteristics, maternal fish and marine n-3 fatty acid intake,
and marine n-3 fatty acid status in maternal and umbilical
cord blood. Am J Clin Nutr 94: 1986S–1992S, 2011.
7. Palm M, Axelsson O, Wernroth L, and Basu S. F2-iso-
prostanes, tocopherols and normal pregnancy. Free Radic Res
43: 546–552, 2009.
8. Shoji H and Koletzko B. Oxidative stress and antioxidant
protection in the perinatal period. Curr Opin Clin Nutr Metab
Care 10: 324–328, 2007.
9. Tara F, Maamouri G, Rayman MP, Ghayour-Mobarhan M,
Sahebkar A, Yazarlu O, Ouladan S, Tavallaie S, Azimi-
Nezhad M, Shakeri MT, Boskabadi H, Oladi M, Sangani MT,
Razavi BS, and Ferns G. Selenium supplementation and the
incidence of preeclampsia in pregnant Iranian women: a
randomized, double-blind, placebo-controlled pilot trial. Tai-
wan J Obstet Gynecol 49: 181–187, 2010.
Address correspondence to:
Dr. Cruz E. Garcı ´a-Rodrı ´guez
Department of Biochemistry and Molecular Biology II
Biomedical Research Center
Institute of Nutrition and Food Technology ‘‘Jose ´ Mataix’’
University of Granada
Avenida del Conocimiento s/n
Date of first submission to ARS Central, January 4, 2012; date
of acceptance, January 4, 2012.
ADS¼antioxidant defense system
FFQ¼food frequency questionnaire
HPLC-EC¼high-pressure liquid chromatography
coupled to an electrochemical detector
n-3 LCPUFA¼n-3 long chain-polyunsaturated fatty
NADPH¼reduced nicotinamide adenine
RBC¼red blood cell
ROS¼reactive oxygen species
SiPS¼Salmon in Pregnancy Study
1406GARCI´A-RODRI´GUEZ ET AL.