Download Status of cis and trans Fatty Acids in Brazilian Adolescent Mothers

Original Study
Status of cis and trans Fatty Acids in Brazilian Adolescent Mothers
and Their Newborns
F.S. Santos MS 1, C.R.M. Chaves PhD 2, R.S.S. Costa PhD 1,2, O.R.C. Oliveira MS 1, M.G. Santana MS 1,
~o BS 1, F.L.C. Sardinha PhD 1, G.V. Veiga PhD 1, M.G. Tavares do Carmo PhD 1,*
F.D. Conceiça
1
2
~o Josu
rio de Bioquımica Nutricional, Instituto de Nutriça
Laborato
e de Castro da Universidade Federal do Rio de Janeiro, RJ, Brazil
~o Oswaldo Cruz, Rio de Janeiro, RJ, Brazil
Instituto Fernandes Figueira da Fundaça
a b s t r a c t
Study Objective: The objective was to quantify cis and trans fatty acids in maternal plasma and infant cord plasma from adolescent mothers.
Design: From 80 adolescent healthy mothers, we sampled postpartum maternal blood and umbilical cord blood at birth. Trans fatty acids
(tFAs), linoleic (18:2), and arachidonic (AA, 20:4) acids of the n-6 family, and a-linolenic (18:3), eicosapentaenoic (20:5) and docosahexaenoic (22:6) acids of the n-3 family were analyzed by gas-liquid chromatography. Results were expressed as a percentage of total fatty
acids.
Results: Linoleic fatty acid was present in greater proportions in the maternal plasma than in that of the umbilical cord, whereas AA was
present in greater proportions in the total lipids of umbilical cord blood. Docosahexaenoic acid was the long-chain polyunsaturated fatty
acid of the n-3 family that was predominant in both maternal and umbilical cord plasma. The tFAs in the maternal plasma had a negative
correlation with oleic acid and linoleic acid. Linolenic acid had a positive correlation with cephalic perimeter upon birth. A tendency for
a negative correlation between trans isomers and gestational age at birth (P 5 .05) was observed.
Conclusions: Long-chain polyunsaturated fatty acids, which are important to fetal growth and development, were found in greater
quantities in the cord blood of newborns of adolescents than in the maternal blood, indicating a priority of transfer of AA and docosahexaenoic fatty acids to the fetus. Despite the lower levels of tFAs found in maternal blood, we verified potential risk for premature birth.
Key Words: Pregnancy, Nutrition, Adolescence, Essential fatty acids, Trans isomers, Newborns, Umbilical cord
Introduction
Fetuses and newborns require an adequate supply of n-6
and n-3 fatty acids, mainly long-chain polyunsaturated fatty
acids (LC-PUFA) such as docosahexaenoic acid (DHA, 22:6
n-3) and arachidonic acid (AA, 20:4 n-6) in order to sustain
development of neurological structures of the brain and
retina and to support normal growth and development of
other tissues.1,2 Moreover, these fatty acids are the precursors of eicosanoids, which are essential constituents of the
membrane lipids that maintain cellular and organelle
integrity and are important intracellular mediators of gene
expression.1,3 Arachidonic acid (n-6) and DHA (n-3) are
derived from dietary essential fatty acids (EFAs) such as
linoleic acid (LA, 18:2 n-6) and linolenic acid (ALA, 18:3 n-3)
by fatty acid desaturases and elongases in the maternal
organism.4 Because of these fundamental roles of EFA and
LC-PUFA, maternal, fetal, and neonatal EFA/LC-PUFA status
is an important determinant of health and disease in
infancy and later life.
Abbreviations: AA, arachidonic acid; AGA, adequate gestational age; ALA, linolenic acid; BMI, body mass index; DHA, docosahexaenoic acid; EFA, essential fatty
acid; EPA, eicosapentaenoic acid; FA, fatty acid; GA, gestational age; LC-PUFA, longchain polyunsaturated fatty acid; LA, linoleic acid; LGA, large for gestational age;
SGA, small for gestational age; tFA, trans-fatty acids.
The authors indicate no conflicts of interest.
*Address correspondence to: Dra. Maria das Graças Tavares do Carmo/ Universidade
de, Instituto de Nutriça
~o Bloco J -2
Federal do Rio de Janeiro / Centro de Ciencias da Sau
andar, 21.9415.90 - Rio de Janeiro e Brasil; Fax: þ55 21 280 83 43
E-mail address: [email protected] (M.G. Tavares do Carmo).
Adolescence is characterized by a period in which dietary
behavior is based on choosing for more attractive, available,
practical, and cheaper food, without much concern for
nutritional quality.5 The habit of consuming excessive
amounts of food rich in fat and industrialized products, like
cookies and ice cream, containing trans fatty acids (tFAs) has
been observed in Brazil.6
Trans fatty acids are found in a variety of processed food
made with partially hydrogenated vegetable oils, and levels
are higher in countries in which hydrogenated vegetable
oils are extensively used by the food industry. Trans fatty
acids from the diet are absorbed and incorporated into
human tissue.7 Before and after birth, exposure to these
fatty acids occurs by placental transfer and through the
mother’s milk.8 Thus, fetal exposure is dependent on the
concentration of the given fatty acid in the maternal plasma,
and thus on maternal dietary intake.
Infant tissues incorporate tFAs, leading to an increase in
tissue levels of linoleic acid and to a relative decrease in the
levels of AA and DHA acids, which suggests that tFA have an
inhibitory effect on the activity of the D3 and D6 desaturase
enzymes.1,9e11 The industrial hydrogenation process causes
the loss of LA, and, particularly of ALA, from food.9,12,13 Thus,
food containing tFAs is often poor in EFAs. Adverse effects
like reduction in weight and fetal growth and greater risk of
pre-eclampsia have been reported in conjunction with
elevated consumption of trans isomers during pregnancy.13
Pregnancy during adolescence accounts for up to onefifth of all births worldwide,14 and it is associated with
ˇ
1083-3188/$ - see front matter Ó 2012 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc.
doi:10.1016/j.jpag.2012.05.001
F.S. Santos et al. / J Pediatr Adolesc Gynecol 25 (2012) 270e276
a variety of negative outcomes for mother and child. In
Brazil, 21% of the babies born in the public health system are
from adolescent mothers.15 Studies of blood concentrations
of tFAs and their relation to plasma levels of EFAs/LC-PUFAS
and maternal characteristics have been conducted in adult
pregnant women.16,17 However, there is a remarkable lack of
similar studies in pregnant adolescents. When pregnancy
and subsequent lactation are superimposed upon adolescence, nutritional risks associated with each condition may
be further enhanced.
The aims of this study were to determine the concentrations of FA in the plasma of pregnant adolescents and the
cord plasma of their newborns. In addition, associations
between FA concentrations and maternal and neonatal
characteristics were also investigated.
Materials and Methods
Study Design and Participants
A cross-sectional survey of a convenience sample of
pregnant adolescents was conducted from August 2010 to
June 2011 in the maternity ward of the Institute Fernandes
~o Oswaldo Cruz (FIOCRUZ), Rio de Janeiro,
Figueira/Fundaça
Brazil, a public health unit of the municipality of Rio de
Janeiro, Brazil, which attends pregnant adolescents at high,
medium, and low risk. The ethics committee of FIOCRUZ
approved the study protocol.
Eighty healthy pregnant adolescents, who met the eligibility criteria and were willing to participate, were enrolled
in the study. The eligibility criteria for participation of the
volunteers in the study were: (1) ages varying from 15-19
years (owing to the high proportion of pregnant teens in this
age group in Brazil18); (2) first and singleton pregnancy; and
(3) not smokers or users of illicit drugs or alcohol. Exclusion
criteria were maternal gestational diabetes, pregnancyinduced hypertension, metabolic or genetic disorders,
infection, and complications during delivery, including
a newborn with congenital malformation. All participants
and/or 1 of their parents or legal guardians signed an
informed consent form prior to enrolment.
A questionnaire was administered to obtain sociodemographic, anthropometric, and obstetric data and information regarding lifestyle. The local nursing staff carried out
anthropometric measurements of infants at delivery. All
other birth outcome variables mentioned in Table 1 were
measured according to standard hospital procedures.
Anthropometric Assessment of Pregnant Adolescents and Newborns
Pre-gestational weight and height measurements were
taken on the first visit to antenatal care, prior to the 14th
gestational week.19 Body mass index (BMI: weight [kg]/
height[m]2) cutoff points specific to adolescents and the
female sex were used for the assessment of nutritional
status of the adolescents.20
The total gestational weight gain was calculated by
subtracting the pre-pregnancy weight from the final weight
immediately before delivery. The adequacy of weight gain
was classified according to recommendations from the
271
Table 1
Sociodemographic, Gynecological, and Anthropometric Characteristics of Pregnant
Adolescents and Their Newborns
Socioeconomic Variables
Per capita family income (n 5 52)
!0.6 minimum wages per capita
$0.6 minimum wages per capita
Do not attend school (n 5 80)
Dropped out because of pregnancy (n 5 41)
Skin color (n 5 80)
White
Brown
Black
Marital status (n 5 80)
Single
Married or stable union
n
%
29
23
41
26
55.8
44.2
51.3
63.4
24
44
12
30.0
55.0
15.0
59
21
73.8
26.2
Gynecological Variables (n 5 80)
n
%
Gynecological age O 2 y
Used contraceptives
Unwanted pregnancy
First-time pregnancy
76
43
57
58
95.0
53.8
71.3
72.5
Maternal Anthropometric Variables (n 5 80)
n
%
Pre-gestational state of nutrition
Underweight
Eutrophic
Overweight/obese
Ponderal gain
Below recommended
Recommended
Over recommended
03
69
08
3.8
86.2
10.0
16
29
31
21.1
38.1
40.8
Anthropometric Variables of Newborn
n
%
6
74
7.5
92.5
26
50
4
32.5
62.5
5.0
4
73
5.0
91.25
47
29
61.8
38.2
61
15
03
77.3
18.9
3.8
Gestational age at birth, wk (n 5 80)
!37
$37
Birth type (n 5 80)
Cesarean
Vaginal
Forceps
Birth wt, g (n 5 80)
!2500
2500-4000
Cephalic perimeter at birth, cm (n 5 76)
!35
$35
Weight/gestational age correlation (n 5 79)
AGA
SGA
LGA
Abbreviations: AGA, adequate for gestational age; LGA, large for gestational age;
SGA, small for gestational age
Institute of Medicine,21 following pre-gestational BMI
categories, as proposed by Gutierrez and King.22
To classify the nutritional status of the newborn, the
gestational weight/age ratio at birth was used according to
criteria defined by Alexander et al.23 The classification of
low birth weight was defined according to the World Health
Organization established cutoff point of weight less than
2500 g.24
Collection of Samples, Preparation, and Analysis
During labor, which lasted 6-12 hours, the women were
not allowed to eat and had an intravenous infusion of
normal saline (no more than 50 mL/h). Epidural analgesia
was not used. Samples of maternal blood were taken from
the antecubital vein (which was not used for infusion)
immediately after delivery (within 30 min after delivery).
Blood samples from the umbilical cord of newborns were
272
F.S. Santos et al. / J Pediatr Adolesc Gynecol 25 (2012) 270e276
collected immediately after the placenta had been expelled.
The samples were collected in tubes containing 1 g Na2EDTA/L. The plasma was separated within 30 minutes
following sampling and kept at e80 C until analyzed. All
determinations were performed in duplicate.
The lipids in the samples were extracted, saponified, and
methylated according to the method described by Lepage
and Roy.25 Fatty acid methyl esters were separated (SP2560
column, Supelco, Bellefonte, PA, USA) and quantified by gasliquid chromatography. The chromatographic conditions
were similar to those described by Tinoco et al.8 The esters
were identified by comparing their retention times to
known standards (Sigma, Supelco). Results were expressed
as mean standard deviation of weight percentage (g/100 g
of total fatty acids). The coefficients of variation for the
analyses were below 5.0% for all FA.
Statistical Analysis
Statistical analysis was performed using the Statistical
Program for the Social Sciences (version 13.0, SPSS, Chicago,
IL, December 2004) and Epi Info (version 6.04, Centers for
Disease Control and Prevention/World Health Organization,
Atlanta, GA, 1996) software.
To evaluate correlations between continuous variables,
the Pearson correlation coefficient was used to investigate
associations between maternal and neonatal FAs and
between characteristics of the newborn infants (gestational
age, weight, length, and head circumference at birth) and
FAs. The continuous variables of the newborns and adolescents were presented in mean, minimum, and maximum
values, and, for categorical variables, in frequencies. For
comparison of the average FA content in the umbilical cord
plasma of neonates and the plasma of adolescent mothers,
the Student t-test was used. Differences were considered
statistically significant at P !.05.
Results
The mean age of the adolescent mothers was 16.8 2.2
years, and the mean age of menarche was 11.7 1.7 years
(Table 1). Around 10% of the population studied was overweight or obese and 4% was underweight, according to their
pre-gestational BMI. Of the 80 participants, 41% gained
more weight than recommended during gestation.
Only 5% of the neonates weighed under 2500 g at birth,
77% were born at a weight that was adequate for their
gestational age, and 7.5% were premature (gestational age
! 37 wk).
The tFA content present in the mothers’ blood and that of
the umbilical cord was under 2% (Table 2). The predominant
n-6 FA in maternal plasma is LA, whereas in umbilical cord
plasma it is AA. Docosahexaenoic acid is the predominant n3 FA, both in maternal and in umbilical cord plasma. In
relation to total saturated FAs, greater proportions were
found in the total lipids of the umbilical cord plasma than in
the maternal plasma (P ! .001; Table 2).
Trans fatty acids in the maternal plasma correlated
negatively with oleic acid (r 5 -0.30, P ! .001), LA (r 5 -0.39,
P ! .001), ALA (r 5 -0.41, P !.001), and eicosapentaenoic
Table 2
Composition of Fatty Acids (%) in Total Lipids from Maternal and Umbilical Cord
Plasma of Pregnant Adolescents and Their Newborns
Fatty acids
Maternal
plasma
Mean
Mono-unsaturated
C18:1 (n-9) cis
C18:1 (n-9) trans
Essential polyunsaturated
C18:2 n-6 (linoleic)
C18:3 n-3 (linolenic)
Long-chain polyunsaturated
C20:4 n-6 (AA)
C22:4 n-6
C20:5 n-3 (EPA)
C22:5 n-3
C22:6 n-3 (DHA)
Total MFAa
Total EFAb
Total n-6 PUFAc
Total n-3 PUFAd
Total LC-PUFAe
Total saturatedf
Total transg
Umbilical Cord
Plasma
P
SD
Mean
SD
16.3
0.7
0.4
0.09
12.8
0.5
0.3
0.07
.06
.07
31.5
0.16
0.4
0.04
12.9
0.5
0.3
0.1
.00
.00
5.6
0.7
0.3
0.2
2.0
19.4
31.8
37.9
4.5
9.5
36.0
0.7
0.1
0.04
0.03
0.03
0.08
0.3
0.4
0.7
0.2
0.1
0.3
0.08
15.3
0.9
0.6
0.3
3.1
20.7
13.4
26.8
2.9
18.5
43.9
0.5
0.3
0.09
0.05
0.1
0.1
0.5
0.3
0.3
0.1
0.4
0.4
0.08
.00
.00
.00
.41
.00
.04
.00
.00
.00
.00
.00
.08
Note. The differences which were considered statistically significant at P !.05 are
shown in bold.
Abbreviations: AA, arachidonic fatty acids; AGM, monounsaturated fatty acids;
AGPI-CL, long-chain polyunsaturated fatty acids; DHA, docosahexaenoic fatty acids;
EFA, essential fatty acids; EPA, eicosapentaenoic fatty acid; PUFA, polyunsaturated
fatty acids
a
Includes all cis isomers of position; b Includes C18:3 n-3 and C18:2 n-6; c Includes
C18:2 n-6, C18:3 n-6, C20:2 n-6, C20:3 n-6, C20:4 n-6 e C22:4 n-6; d Includes C18:3
n-3, C20:5 n-3, C22:5 n-3 and C22:6 n-3; e Includes EPA, DHA and ARA; f Total
saturated includes C14:0, C15:0, C16:0 and C18:0; g Total trans includes C 18:1 n-9
trans and C 18:2 n-6 trans
acid (EPA; r 5 - 0.35, P ! .001). In the umbilical cord plasma,
a negative correlation was found between AA and LA
(r 5 0.31, P ! .001; Table 3). Pre-gestational BMI correlated
negatively with oleic acid content (r 5 0.28, P ! .02; Table 4).
The LA content and total saturated FAs correlated positively
with the cephalic perimeter and length at birth, respectively
(r 5 0.29, P ! .03 and r 5 0.33, P ! .01). Total tFA tended to
correlate negatively with the gestational age at birth (r 5 - 0.25,
P ! .05; Table 5).
Discussion
Compared with international studies, in which these
isomers were investigated in human milk and/or blood
from adult mothers, lower levels of tFAs were found in our
study.17,26,27 Moreover, we found no difference between
concentrations of tFAs in maternal and umbilical cord
plasma, although lower levels had been found in the plasma
of the umbilical cord. Other authors also noted the presence
of tFAs in the cord plasma at lower percentages than those
observed in the mothers’ blood.28,29 One can suppose
selective placental transfer of tFAs may have occurred, since
they are not synthesized in fetal tissue and originate from
the mother’s diet.
Children and adolescents have consumption patterns
that are different from those of adults.6 Most of the types of
food in which tFAs are available, such as french fries, snacks,
cookies, and breads, are also popular among children
and adolescents. On the other hand, our recent findings
indicate qualitative modifications in the dietary intake of
F.S. Santos et al. / J Pediatr Adolesc Gynecol 25 (2012) 270e276
273
Table 3
Pearson Correlation Coefficient for Ratio between Fatty Acids in Plasma of Mother and Umbilical Cord
Fatty Acids
C18:1 n-9
cis
C18:1 n-9
trans
C18:2 n-6
C18:3 n-3
C20:4 n-6
(AA)
C22:4 n-6
C20:5 n-3
(EPA)
C22:5 n-3
C22:6 n-3
(DHA)
Maternal Plasma
MFAd
C18:1 (n-9) cis (Oleic)
C18:1 (n-9) trans
EFAe
C18:2 n-6 (Linoleic)
C18:3 n-3 (Linolenic)
LC-PUFAf
C20:4 n-6 (AA)a
C22:4 n-6
C20:5 n-3 (EPA)b
C22:5 n-3
C22:6 n-3 (DHA)c
Total saturatedg
Fatty acids
r
0.30
P
.00
r
0.03
-
P
.81
-
r
0.27
0.39
P
.02
.00
r
0.09
0.41
P
.46
.00
r
0.54
0.08
P
.00
.48
r
0.67
0.12
P
.00
.30
r
0.03
0.35
P
.07
.00
r
0.32
0.41
P
.01
.00
r
0.19
0.20
P
.11
.08
0.27
0.09
.02
.46
0.39
0.41
.00
.00
0.16
.17
0.16
-
.17
-
0.07
0.19
.54
.10
0.23
0.16
.05
.19
0.46
0.27
.00
.02
0.38
0.47
.00
.00
0.24
0.14
.04
.23
0.54
0.67
0.04
0.32
0.19
0.24
.00
.00
.78
.01
.11
.04
0.08
0.12
0.35
0.41
0.20
0.20
.48
.31
.00
.00
.08
.09
0.07
0.23
0.46
0.38
0.24
0.67
.54
.05
.00
.00
.04
.00
0.19
0.16
0.27
0.47
0.14
0.06
.10
.19
.02
.00
.23
.60
0.49
0.05
0.32
0.02
0.11
.00
.67
.00
.84
.34
0.49
0.11
0.32
0.13
0.02
.00
.37
.01
.27
.87
0.05
0.11
0.30
0.14
0.20
.67
.37
.01
.24
.09
0.32
0.32
0.31
0.24
0.12
.00
.01
.01
.04
.29
0.02
0.13
0.14
0.24
0.02
.84
.27
.24
.04
.88
C18:1 n-9
cis
C18:1 n-9
trans
C18:2 n-6
C18:3 n-3
C20:4 n-6
(AA)
C22:4 n-6
C20:5 n-3
(EPA)
C22:5 n-3
C22:6 n-3
(DHA)
Umbilical Cord Plasma
MFAd
C18:1 (n-9) cis (oleic)
C18:1 (n-9) trans
EFAe
C18:2 n-6 (Linoleic)
C18:3 n-3 (Linolenic)
LC-PUFAf
C20:4 n-6 (AA)a
C22:4 n-6
C20:5 n-3 (EPA)b
C22:5 n-3
C22:6 n-3 (DHA)c
Total saturatedg
r
0.12
P
.37
r
0.12
-
P
.37
-
r
0.20
0.10
P
.12
.44
r
0.21
0.20
P
.11
.13
r
0.23
0.17
P
.08
.19
r
0.02
0.13
P
.87
.33
r
0.18
0.11
P
.16
.39
r
0.18
0.02
P
.18
.89
r
0.27
0.13
P
.03
.33
0.20
0.21
.12
.11
0.10
0.20
.44
.13
0.09
.05
0.09
-
.50
-
0.31
0.31
.01
.02
0.12
0.25
.35
.06
0.18
0.49
.17
.00
0.06
0.44
.64
.00
0.40
0.11
.00
.42
0.23
0.02
0.18
0.18
0.28
0.21
.08
.87
.16
.18
.03
.11
0.18
0.13
0.11
0.02
0.13
0.16
.17
.32
.39
.89
.34
.24
0.31
0.34
0.12
0.18
0.06
0.06
.01
.01
.35
.17
.64
.64
0.31
0.25
0.49
0.44
0.11
0.19
.02
.06
.00
.00
.42
.14
0.22
0.29
0.17
0.18
0.29
.09
.03
.20
.17
.03
0.22
0.52
0.00
0.29
0.62
.09
.00
.99
.03
.00
0.29
0.52
0.19
0.14
0.46
.03
.00
.15
.27
.00
0.17
0.00
0.19
0.01
0.26
.20
.99
.15
.93
.05
0.18
0.29
0.14
0.01
0.31
.17
.03
.27
.93
.02
Abbreviations: AA, arachidonic fatty acid; DHA, docosahexaenoic fatty acid; EFA, essential fatty acids; EPA, eicosapentaenoic fatty acid; LC-PUFA, long-chain polyunsaturated
fatty acids; MFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids
d
MFA: monounsaturated fatty acids-Includes all cis isomers of position; eEFA: essential fatty acids - Includes C18:3 n-3 and C18:2 n-6; fLC-PUFA: polyunsaturated fatty
acids - Includes C20:4 n-6 (AA), C22:4 n-6; C20:5 n-3 (EPA), C22:5 n-3 and C22:6 n-3 (DHA); gTotal saturated includes C14:0, C15:0, C16:0 and C18:0
a
AA e arachidonic fatty acid
b
EPA e eicosapentaenoic fatty acid
c
DHA e docosahexaenoic fatty acid
adolescents during pregnancy, since 77% reported that they
had changed their eating habits. Of this number, 59%
reported having reduced their consumption of processed
products (data not shown). This finding offers a possible
explanation for the reduced levels of tFA observed in plasma
of the pregnant adolescents studied.
One other possible reason for the lower levels of tFAs in
maternal and umbilical cord plasma observed in the present
study may be associated with the reduction in tFA content in
processed products in Brazil. A recent reduction in the use of
partially hydrogenated fats that has been adopted by the
food industry has resulted in a drop in consumption of tFAs
in many countries.13,30 In Brazil, in seeking to contribute to
the reduced consumption of these isomers, the National
Sanitary Surveillance Agency (Agencia Nacional de Vigiria/ANVISA) published, on December 23, 2003,
lancia Sanita
RDC Resolution no. 360 (Technical regulation on the nutritional labeling of packaged foods), which amounts to the
obligatory declaration of the quantity of trans fats on food
labels; the established deadline for meeting the requirements of the new legislation was July 31, 2006.31 Recent
implementation of proper technological processing in
Brazilian industries with the aim of reducing the formation
of tFAs was probably a direct consequence of the requirements of the present legislation. Thus, RDC resolution 360
constitutes an important instrument for implementing
public policy destined to promote the population’s consumption of healthier food.
On the other hand, the technical regulation about
nutritional labeling in Brazil (RDC 360/2003),31 in effect
since July 2006, is not applied to companies that commercialize prepared and ready-to-eat food. Therefore, fast food
may be a potential source of tFAs, but companies are not
obligated to inform consumers. The analysis carried out
by Aued-Pimentel et al identified that total or partial
consumption of those food items is capable of providing tFA
consumption above the maximum values recommended by
the World Health Organization,32 which suggests that daily
tFA consumption should be kept below 1% of total energy
intake. For adults who consume 2000 kcal/d, the maximum
acceptable value for tFA consumption should not exceed 2
g/d. These recommendations aim to contribute to the
reduction in risk of developing chronic diseases.33
LC-PUFAs (DHA and AA) were shown to be in greater
proportions in plasma of the umbilical cord in relation to
the levels present in maternal plasma (Table 2). On the
other hand, total EFA (LA and ALA) was significantly lower
in the umbilical cord blood than in the maternal plasma.
These results suggest that placental transfer is selectively
greater for LC-PUFAs than for EFAs. Similar data have been
ˇ
ˇ
274
F.S. Santos et al. / J Pediatr Adolesc Gynecol 25 (2012) 270e276
Table 4
Pearson Correlation Coefficient for Ratio between Fatty Acids, Stature, Pre-gestational Body Mass Index, Gestational Ponderal Gain, and Gestational Age in Maternal Plasma of
Pregnant Adolescents
Fatty Acids
Stature
r
Mono-unsaturated
C18:1 (n-9) cis (Oleic)
C18:1 (n-9) trans
Essential polyunsaturated
C18:2 n-6 (Linoleic)
C18:3 n-3 (Linolenic)
Long-chain polyunsaturated
C20:4 n-6 (AA)
C22:4 n-6
C20:5 n-3 (EPA)
C22:5 n-3
C22:6 n-3 (DHA)
Total MFAa
Total EFAb
Total n-6 PUFAc
Total n-3 PUFAd
Total LC-PUFAe
Total saturatedf
Total transg
PG BMI
Ponderal Gain
Gestational Age
P
r
P
r
P
r
P
0.07
0.03
.55
.77
0.28
0.05
.02*
.66
0.01
0.06
.94
.62
0.15
0.19
.22
.09
0.02
0.07
.86
.54
0.00
0.21
.99
.08
0.01
0.20
.93
.08
0.00
0.17
.95
.14
0.02
0.03
0.09
0.01
0.04
0.14
0.01
0.02
0.05
0.01
0.11
0.01
.87
.81
.44
.96
.72
.25
.96
.88
.67
.94
.34
.92
0.18
0.17
0.03
0.19
0.06
0.33
0.04
0.07
0.12
0.18
0.19
0.07
.12
.14
.79
.11
.59
.00**
.75
.55
.33
.13
.11
.54
0.02
0.07
0.02
0.09
0.02
0.01
0.07
0.00
0.09
0.01
0.04
0.00
.84
.59
.89
.48
.86
.94
.55
.98
.45
.95
.19
.97
0.02
0.12
0.05
0.05
0.01
0.16
0.02
0.02
0.07
0.05
0.11
0.18
.89
.69
.70
.69
.92
.17
.86
.84
.56
.68
.33
.33
Note. The differences which were considered statistically significant at P !.05 are shown in bold.
Abbreviations: AA, arachidonic fatty acid; DHA, docosahexaenoic fatty acid; EFA, essential fatty acids; EPA, eicosapentaenoic fatty acid; LC-PUFA, long-chain polyunsaturated
fatty acids; PUFA, polyunsaturated fatty acids
* P ! .05
** P ! .01
a
Includes all cis isomers of position
b
Includes C18:3 n-3 and C18:2 n-6
c
Includes C18:2 n-6, C18:3 n-6, C20:2 n-6, C20:3 n-6, C20:4 n-6 and C22:4 n-6
d
Includes C18:3 n-3, C20:5 n-3, C22:5 n-3 and C22:6 n-3
e
Includes: EPA, DHA and AA
f
Total saturated includes C14:0, C15:0, C16:0 and C18:0
g
Total trans includes C 18:1 n-9 trans and C 18:2 n-6 trans
described before.30,34,35 In this sense, preferential transfer
of particular LC-PUFAs from the maternal to the fetal
circulation in relation to the transfer of EFAs may represent
a determining factor in adequate fetal growth and development. Maintaining adequate transfer of DHA to fetal
blood seems to be an important physiological process, since
humans, even newborns and children, convert less than 1%
of ALA n-3 into DHA n-3.36
Despite the lower levels of tFAs found in maternal blood,
we verified that there was a negative association between
these isomers and oleic acid (r 5 -0.30, P ! .001), LA
(r 5 -0.39, P ! .001), ALA (r 5 -0.41, P ! .001), and EPA
(r 5 - 0.35, P ! .001). Similar results were also revealed by
other authors.3,11,27,37 The most likely hypotheses justifying
these associations involve: (1) a possible inhibiting effect of
tFAs in the desaturation and elongation processes of the n-6
family of FAs, or (2) lower consumption of lipid sources rich
in n-6 and n-3, owing to greater consumption of food rich in
tFAs. On the other hand, in cord plasma, a negative correlation was found between AA and LA (r 5 -0.31, P 5 .01).
Koletzko found inverse associations between tFA and
LC-PUFAs (AA and DHA) in umbilical cord plasma and
between tFAs and birth weight of premature babies.10
Similar to the results reported by Decsi et al,27 our results
revealed no correlations between tFA levels and newborns’
anthropometric parameters (weight, length, and cephalic
perimeter at birth). However, tFAs tended to correlate
negatively with gestational age at birth (P 5 .05). Hornstra
et al,37 while investigating associations between elaidic tFA
(C18:1 trans) levels in plasma, arterial, and venous blood
from the umbilical cord and weight, length, and cephalic
perimeter upon birth, found negative and statistically
significant associations between plasmatic tFAs, cephalic
perimeter, and length upon birth. Elias and Innis examined
70 newborns from adult pregnancy and investigated the
relationship between birth weight, birth length, and length
of gestation and the levels of tFAs in umbilical cord plasma;
those authors found a significant inverse relationship
between the newborn infant plasma concentration of tFAs
in cholesteryl esters and the length of gestation.38 Thus,
based on the literature, and in accordance with our findings,
it is suggested that even in low concentrations, tFAs may
contribute to premature birth.
The results of the present study do not suggest an important correlation between tFAs and gestational age, but
because dietary trans intake in the studied population was
relatively low (59% reported reduced consumption of processed products), we cannot exclude a possible strong negative association at higher intake. Pregnancy in young mothers
is considered to be of the most important risk conditions, not
only because of young age, but also because of economic
problems, lack of education, and insufficient prenatal care. In
this group, the risk of maternal or neonatal complications is
increased,39 and nutrition is an important aspect of prenatal
care. Presence of tFAs in blood may indicate a high risk of
nutritional problems in the young mother and therefore
requires in-depth nutritional assessment, counseling, and
follow-up. Maternal health habits during pregnancy may be
F.S. Santos et al. / J Pediatr Adolesc Gynecol 25 (2012) 270e276
275
Table 5
Pearson Correlation Coefficient for Ratio between Umbilical Cord Plasma Fatty Acids and Newborns’ Anthropometric Data
Fatty Acids
Monounsaturated
C18:1 (n-9) cis (oleic)
C18:1 (n-9) trans
Essential polyunsaturated
C18:2 n-6 (linoleic)
C18:3 n-3 (linolenic)
Long-chain polyunsaturated
C20:4 n-6 (AA)
C22:4 n-6
C20:5 n-3 (EPA)
C22:5 n-3
C22:6 n-3 (DHA)
Total MFAa
Total EFAb
Total n-6 PUFAc
Total n-3 PUFAd
Total dos LC-PUFAe
Total saturatedf
Total transg
Weight
Length
Cephalic Perimeter
Gestational Age
r
P
r
P
r
P
r
P
0.07
0.15
.62
.27
0.07
0.12
.63
.36
0.06
0.01
.68
.96
0.07
0.24
.62
.07
0.02
0.03
.89
.81
0.21
0.07
.11
.63
0.09
0.29
.52
.03*
0.10
0.04
.46
.76
0.10
0.09
0.17
0.11
0.15
0.02
0.02
0.06
0.18
0.15
0.16
0.19
.44
.49
.19
.41
.27
.87
.88
.63
.18
.25
.24
.16
0.04
0.21
0.21
0.21
0.23
0.82
0.05
0.01
L0.30
0.22
0.33
0.10
.76
.11
.12
.12
.08
.54
.71
.97
.02*
.10
.01*
.45
.13
.54
.84
.81
.22
.68
.09
.49
.90
.07
.29
.61
0.12
0.01
0.08
0.07
0.02
0.04
0.13
0.01
0.06
0.08
0.10
0.25
.38
.94
.55
.58
.86
.76
.34
.93
.67
.57
.44
.05
0.20
0.08
0.03
0.03
0.27
0.06
0.22
0.09
0.02
0.24
0.14
0.07
Note. The differences which were considered statistically significant at P !.05 are shown in bold.
Abbreviations: AA, arachidonic fatty acid; DHA, docosahexaenoic fatty acid; EFA, essential fatty acids; EPA, eicosapentaenoic fatty acid; LC-PUFA, long-chain polyunsaturated
fatty acids; MFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids
* P ! .05
a
Includes all cis isomers of position
b
Includes C18:3 n-3 and C18:2 n-6
c
Includes C18:2 n-6, C18:3 n-6, C20:2 n-6, C20:3 n-6, C20:4 n-6 and C22:4 n-6
d
Includes C18:3 n-3, C20:5 n-3, C22:5 n-3 and C22:6 n-3
e
Includes: EPA, DHA and AA
f
Total saturated includes C14:0, C15:0, C16:0 and C18:0
g
Total trans includes C 18:1 n-9 trans and C 18:2 n-6 trans
a major factor for clinical intervention. Moreover, considering
the adolescent’s desire to maximize the health of her developing fetus, poor habits and behaviors may be changed more
easily during pregnancy than at other times.
In summary, our study demonstrates higher plasma LCPUFAs (AA and DHA) in the umbilical cord plasma of
newborns of adolescent mothers compared to maternal
plasma, indicating the occurrence of priority transfer of AA
n-6 and DHA n-3 FAs to the fetus. There was no difference
between tFAs in maternal plasma and in umbilical cord, and
a tendency was observed for these FAs to have a negative
correlation with gestational age at birth. Given the harmful
effects of tFAs on health, action should be taken to reduce
consumption of these fatty acids during pregnancy.
Acknowledgments
This research is based on data from the Brazilian study
“Trans fatty acids in pregnant adolescents and its consequences for maternal and child health,” which was funded
primarily by the Brazilian Research Council (Conselho
gicoNacional de Desenvolvimento Cientıfico e Tecnolo
~o de Amparo a Pesquisa do Rio de
CNPq) and Fundaça
Janeiro (FAPERJ).
References
1. Innis SM: Fatty acids and early human development. Early Hum Dev 2007;
83:761
2. Innis SM: Dietary n-3 fatty acids and brain development. J Nutr 2007; 137:855
3. Herrera E: Implications of dietary fatty acids during pregnancy on placental,
fetal and postnatal development da review. Placenta 2002; 23:S19
4. Das UN: Essential fatty acidsda review. Curr Pharm Biotechnol 2006; 7:467
5. Story M, Moe J: Eating behaviors and nutritional implications. In: Story M,
Stang J, editors. Nutrition and the Pregnant Adolescent: A Practical Reference
Guide. Minneapolis, MN, School of Public Health, University of Minnesota,
2000, pp 47e54
6. Chiara VL, Sichieri R: Dietary consumption in adolescents: simplified
questionnaire for assessing cardiovascular risk. Arq Bras Cardiol 2001; 77:337
7. Micha R, Mozaffarian D: Trans fatty acids: effects on cardiometabolic health and
implications for policy. Prostaglandins Leukot Essent Fatty Acids 2008; 79:147
8. Tinoco SMB, Sichieri R, Setta CL, et al: Trans fatty acids from milk of Brazilian
mothers of premature infants. J Paediatr Child Health 2008; 44:50
9. Kirstein D, Hoy CE, Holmer G: Effect of dietary fats on the delta-6-desaturation and
delta-5-desaturation of fatty-acids in rat-liver microsomes. Br J Nutr 1983; 50:749
10. Koletzko B: Trans fatty acids may impair biosynthesis on long-chain polyunsaturates and growth in man. Acta Paediatr 1992; 81:302
11. Decsi T, Koletzko B: Do trans fatty acids impair linoleic acid metabolism in
children? Ann Nutr Metab 1995; 39:36
12. Innis SM, Green TJ, Halsey TK: Variability in the trans fatty acid content of foods
within a food category: implications for estimation of dietary trans fatty acid
intakes. J Am Coll Nutr 1999; 18:255
13. Innis SM: Trans fatty intakes during pregnancy, infancy and early childhood.
Atheroscler Suppl 2006; 7:17
14. Population Reference Bureau. The World's Youth. 2000. Available at: http://www.
prb.org/Reports/2000/WorldsYouth2000.aspx. Accessed November 28, 2011.
rio da Sau
de. Datasus. Sinasc. Sistema de Informaço
~es sobre Nascidos Vivos.
15. Ministe
Brasil: Datasus/MS/SVS/DASIS; 2003. http://tabnet.datasus.gov.br. Jan 16, 2012
€ ller J: Cis- and trans-isomeric fatty acids in plasma lipids of
16. Koletzko B, Mu
newborn infants and their mothers. Biol Neonate 1990; 57:172
17. Innis SM, King DJ: Trans fatty acids in human milk are inversely associated with
concentrations of essential all-cis n-6 and n-3 fatty acids and determine trans,
but not n-6 and n-3, fatty acids in plasma lipids of breast-fed infants. Am J Clin
Nutr 1999; 70:383
18. Silva VC, Barbieri M, Aperibense PGGS, Santos CRGC: Pregnancy in adolescence
in units of public health in Brazil: an integrative literature review. Adolesc
Saude 2010; 7:60e7
19. Ministry of Health (MH): Prenatal care: Secretary of Health Policy. Brasılia (DF);
2000. http://bvsms.saude.gov.br/bvs/publicacoes/cd04_11.pdf. Accessed Feb 2, 2012
20. CDC: National Center for Health Statistics/National Center for Chronic Disease
Prevention and Health Promotion 2000. http://www.cdc.gov/growthcharts.
Accessed March 19, 2012.
21. Institute of Medicine e IOM: Weight Gain During Pregnancy: Reexamining the
Guidelines. National Academy of Science. Washington, National Academy Press,
2009
22. Gutierrez Y, King JC: Nutrition during teenage pregnancy. Pediatr Ann 1993;
22:99e108
276
F.S. Santos et al. / J Pediatr Adolesc Gynecol 25 (2012) 270e276
23. Alexander GR, Himes JH, Kaufman RB, et al: A United States national reference
for fetal growth. Obstet Gynecol 1996; 87:163
24. World Health Organization (WHO): Physical status: the use and interpretation
of anthropometry. Geneva, Switzerland; 1995. Technical Report Series 854
25. Lepage G, Roy CC: Direct transesterification of all classes of lipids in a one-step
reaction. J Lipid Res 1987; 27:114
26. Koletzko B, Mrotzek M, Bremer HJ: Fatty acid composition of mature human
milk in germany. Am J Clin Nutr 1988; 47:954
27. Decsi T, Burus I, Moln
ar S, et al: Inverse association between trans isomeric and
long-chain polyunsaturated fatty acids in cord blood lipids of full-term infants.
Am J Clin Nutr 2001; 74:364
28. Mojska H: Influence of trans fatty acids on infant and fetus development. Acta
Microbiol Pol 2003; 52:67
29. Vlaardingerbroek H, Hornstra G: Essential fatty acids in erythrocyte
phospholipids during pregnancy and at delivery in mothers and their
neonates: comparison with plasma phospholipids. Prostaglandins Leukot
Essent Fatty Acids 2004; 71:363
30. Craig-Schmidt MC: World-wide consumption of trans fatty acids. Atheroscler
Suppl 2006; 7:1
31. ANVISA. The National Sanitary Surveillance Agency. Ministry of Health.
Foods e Obligatory Nutritional Labelling of Foods. RDC Resolution no. 360
http://www.anvisa.gov.br/legis/resol/2003/rdc/360_03rdc.htm. Accessed March
5, 2012
32. Aued-Pimentel S, Silva SA, Kus MMM, et al: Evaluation of total fat, saturated and
trans fatty acids in foodstuffs with the claim “trans free. Braz J Food Technol, VII
BMCFB, 2009, Available at: http://bjft.ital.sp.gov.br/artigos/especiais/especial_
2009_2/v12ne_t0102.pdf
33. World Health Organization. Recommendations for preventing cardiovascular
diseases. http://www.who.int/dietphysicalactivity/publications/trs916/en/gsfao_
cvds.pdf. Accessed November 28, 2011
34. De Vriese SR, Matthys C, De Henauw S, et al: Maternal and umbilical fatty acid
status in relation to maternal diet. Prostaglandins Leukot Essent Fatty Acids
2002; 67:389
35. Georgieff MK, Innis SM: Controversial nutrients that potentially affect preterm
neurodevelopment: essential fatty acids and iron. Pediatr Res 2005; 57:99
36. Uauy R, Mena P, Wegher B, et al: Long chain polyunsaturated fatty acid
formation in neonates, effect of gestational age and intrauterine growth.
Pediatr Res 2000; 47:127
37. Hornstra G, Eijsden MV, Dirix C, et al: Trans fatty acids and birth outcome:
some first results of the MEFAB and ABCD cohorts. Atheroscler Suppl
2006; 7:21
38. Elias SL, Innis SM: 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 2001; 3:807
39. Zuckerman B, Alpert JJ, Dooling E, et al: Neonatal outcome: is adolescent
pregnancy a risk factor? Pediatrics 1983; 71:489