J. Obstet. Gynaecol. Res. Vol. 38, No.

3: 498504, March 2012

doi:10.1111/j.1447-0756.2011.01763.x

Nutritional status among women with pre-eclampsia and

healthy pregnant and non-pregnant women in a Latin
American country
jog_1763

498..504

Laura Reyes1*, Ronald Garcia1, Silvia Ruiz1, Mahshid Dehghan4 and

Patricio Lpez-Jaramillo2,3
1

Fundacin Cardiovascular de Colombia, 2Fundacin Oftalmolgica de Santander-Clnica Carlos Ardila Lulle (FOSCAL),
Floridablanca, and 3Universidad de Santander, UDES, Bucaramanga, Santander, Colombia; and 4Population Health Research
Institute, McMaster University, Hamilton, Ontario, Canada

Abstract
Aims: Pre-eclampsia (PE) is one of the leading causes of maternal and perinatal morbidity and mortality
worldwide. It has been proposed that, among other risk factors, the nutritional status of women can lead to the
endothelial dysfunction that characterizes this entity. The aim of the present study was to compare the
nutritional status of women with PE with healthy pregnant and non-pregnant women.
Material and Methods: A multicenter casecontrol study was carried out. Between September 2006 and July
2009, 201 women with PE were compared with 201 pregnant, and 201 non-pregnant aged-matched women
without cardiovascular or endocrine diseases. A clinical history and physical examination was performed.
Fasting blood samples were drawn to measure serum glucose and lipid profile. The nutritional status of
participants was assessed using a food frequency questionnaire.
Results: The average age of women was 26.6 7.2 years. Compared to healthy pregnant controls, women with
PE had a higher body mass index, higher fasting blood glucose levels, higher triglycerides, and lower
high-density lipoprotein cholesterol levels. Women with PE had a higher intake of carbohydrates, energy
intake and cereal compared to healthy pregnant and non-pregnant controls. A conditional logistic regression
demonstrated that carbohydrate and sodium intake are associated with PE development.
Conclusions: Diets of women with PE were characterized by higher energy and carbohydrate intake compared to normal pregnant and non-pregnant women. This suggests that higher carbohydrate and sodium
intake increases the risk of PE among women in Colombia.
Key words: developing country, energy intake, food intake, nutrition, pre-eclampsia.

Introduction
Pre-eclampsia (PE) affects 510% of pregnancies and is
one of the leading causes of maternal and perinatal
morbidity and mortality worldwide.1,2 It has been postulated that PE is a disorder that arises due to multiple

causes and that nutritional, environmental, socioeconomic, inflammatory, and genetic risk factors may contribute to an alteration of endothelial function, which is
characteristic of the disorder.3
The alteration of endothelial function may involve the production of messenger molecules and

Received: May 7 2011.

Accepted: May 12 2011.
Reprint request to: Professor Patricio Lpez-Jaramillo, Fundacin Oftalmolgica de Santander-Clnica Carlos Ardila Lulle (FOSCAL),
Calle 155A N. 23-09, Urbanizacin El Bosque, Floridablanca, Santander, Colombia. Email: jplopezj@gmail.com;
investigaciones@foscal.com.co
*Laura Reyes is now at University of Alberta, Edmonton, Alberta, Canada.
Silvia Ruiz is now at Universidade de So Paulo, Ribeiro Preto, So Paulo, Brazil.

498

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Nutritional status of Colombian women

consequently the expression of proinflammatory adhesion molecules. These pathways are known to be key
factors in the initiation and progression of the atherogenic process that underlies some cardiovascular
diseases.4
A large body of evidence has shown that some nutrients can improve endothelial function,57 either by
reducing oxidative stress5,6 or by modifying certain
inflammatory responses.7 In addition, multiple studies
have assessed the role of diet in the prevention of
cardiovascular diseases, such as hypertension,8 myocardial infarction9 and diabetes.10 Clausen et al.11 demonstrated that in the second trimester, an increased
intake of energy, sucrose and polyunsaturated fatty
acids were associated with an increased risk of developing PE. On the other hand, an inverse association
was observed between dietary patterns characterized
by a high intake of vegetables, plant foods and vegetable oils and the risk of developing PE.12,13 It has also
been shown that calcium supplementation during
pregnancy, in populations with a history of a low
intake of this mineral, was useful in preventing the
development of pregnancy-induced hypertension and
PE.1416
Nutrition transition and urbanization, which is
observed in developing countries, may partly explain
the epidemic of cardio-metabolic disease,3 increased
risk of gestational diabetes,17 and PE.18 The objective of
this study was to compare the nutritional status of
women with PE with that of healthy pregnant and
non-pregnant women in Colombia.

Methods
Participants
A multicenter casecontrol study was conducted
between September 2006 and July 2009 in six Colombian cities (Bucaramanga, Medelln, Envigado, Ccuta,
Barranquilla, and Santa Marta). PE was defined as the
development of hypertension (blood pressure 140/
90 mmHg) after the 20th week of gestation in women
known to be normotensive beforehand; and the presence of proteinuria (urinary protein 300 mg in a 24-h
period or 1 + on a dipstick in at least two random
urine samples taken at least 46 h apart).19,20 A consecutive convenient sample of pregnant and non-pregnant
controls, matched by age (3 years), was selected from
the same city of residence and the same hospital of
delivery as the women with PE. Non-pregnant controls
were recruited after the enrollment of each woman
with PE, and attended scheduled appointments for

their clinical assessment and their biochemical determinations. The presence of any of the following conditions (before or during pregnancy) was considered as
exclusion criteria for all the participants: chronic hypertension, autoimmune diseases, endocrine diseases,
renal diseases, cancer, HIV or mental illness. The
Institutional Ethics Review Board of the Colombian
Cardiovascular Foundation, Bucaramanga, Colombia,
approved the study. Written informed consent was
obtained from all study participants.

Clinical assessment
For each woman enrolled in the study, a complete clinical history was recorded, using standardized formats,
before the delivery. Standard measurements were performed in duplicate by the same examiner on each
woman. All physical measurements were taken with
women wearing light clothes and without shoes.
Nutritional assessments
Participants dietary intake was assessed using a validated food frequency questionnaire (FFQ).21 The FFQ
included 90 food items traditionally consumed in
Colombia with their standard portion sizes. Foods
were classified into the following food categories: milk
and dairy products, fruits, vegetables, meat, cereals,
mixed dishes, beverages, and desserts. Intake frequencies for the food items consisted of nine categories
ranging from never/once a month to more than six
times per day. Before delivery, trained interviewers
asked participants how often they had consumed one
portion of each food item during the entire previous
year. To compute the total amount of food intake per
day, the reported frequency of consumption for each
food item was multiplied by the portion size and then
total food intake was converted to nutrient intake
based on the foods nutrient profile.
Nutrient database and recipe analysis
A food composition database for nutrient estimation
was developed. The nutrient database was mainly
based on the US Department of Agriculture food composition database and modified with reference to local
food composition tables; this was supplemented with
recipes of locally prepared mixed dishes.22
Biochemical determinations
Blood samples were drawn in fasting conditions (6 h),
from the antecubital vein. Ethylenediaminetetraacetic
acid plasma was separated by centrifugation at
3000 r.p.m. for 15 min and then frozen at -70C and

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L. Reyes et al.

stored until analysis. Glucose concentration and lipid

profile (high-density lipoprotein [HDL], low-density
lipoprotein [LDL], very-low-density lipoprotein
[VLDL] and triglycerides [TG]) were determined by an
enzyme colorimetric test.

Statistical analysis
Descriptive data are expressed as means and standard
deviations (SD). The ShapiroWilk test was used to
assess the normality of continuous data. Continuous
variables were analyzed using two-sample t-tests or the
MannWhitney U-test (for non-normally distributed
data). Categorical variables were analyzed using the
c2-test or Fishers exact test. Statistical significance was
defined as P < 0.05. When more than two groups were
compared, either anova or KruskalWallis analysis was
used, depending on the distribution of variables.
The distribution of nutrient intake was assessed
using a boxplot and the data were found to be skewed.
The data were then log transformed and analyses were
conducted. A Bonferroni correction was used to determine the differences in food intake among the groups.
A conditional logistic regression model was conducted to explore which factors were associated with
the development of PE compared to healthy pregnant
women. Initially, we explored the variables that were
not related to diet, such as gestational age, body mass
index (BMI), the difference between household income
and household outcome and prenatal care assistance.
Variables that were associated with the development of
PE were taken as relevant variables for the adjustment
of estimates of each nutrient. The fiber and carbohydrate intake showed a linear correlation consistent
with the event, so they were maintained as continuous.
On the other hand, the sodium and vitamin C intake
were associated with the development of PE; but in a
non-linear way, thus cut-off points for sodium
(>2200 mg) and for vitamin C (>200 mg) were established. Results were reported as odds ratio (OR) with
95% confidence interval around the estimate. All data
were analyzed using stata statistical software 10.0.

Results
From September 2006 to July 2009, 201 PE cases, 201
healthy pregnant and 201 healthy non-pregnant
women were recruited for the study. The majority of
participants (89.9%) were from urban settings. In comparison with controls (pregnant and non-pregnant
women), women with PE had the lowest household
income per month ($US475.2610.9 [women with PE]

500

vs $US556.5722.9 [pregnant controls] vs $627.9807.3

[non-pregnant controls]; P = 0.001), the lowest household expenditure per month ($US173.6205.4 [women
with PE] vs $US179.5227.1 [pregnant controls] vs
$US200.8239.3 [non-pregnant controls]; P = 0.01) and
the lowest difference between household income
and household expenditure ($US279.7401 [women
with PE] vs $US353.7500.9 [pregnant controls] vs
$US412.1576.6 [non-pregnant controls]; P = 0.001).
Table 1 describes the characteristics of the participants. The average age of women across all groups was
26.63 7.15 years. The gestational age was greater in
healthy pregnant women than in women with PE
(37.6 3.47 weeks vs 34 4.21 weeks; P < 0.0001).
Compared with controls, women with PE were heavier
with an increased BMI; we also observed that 21.5% of
non-pregnant women were overweight (Table 1).
Women with PE had higher heart rates and fasting
blood glucose concentration compared to healthy pregnant and non-pregnant women (Table 1). With regards
to lipid profile, it was observed that women with PE
had lower HDL and LDL cholesterol levels compared
to healthy pregnant women. Additionally, it was noted
that women with PE had higher triglyceride levels
compared to healthy pregnant and non-pregnant
women (Table 1).
Table 2 presents daily intake of energy, macronutrients, selected micronutrients and food groups. It was
found that women with PE had higher energy and
carbohydrate intake compared to healthy pregnant and
non-pregnant controls. Protein and fat intake were
lower among women with PE than in healthy pregnant
women but the difference was not statistically significant. Women with PE had a higher consumption of
cereal compared to healthy pregnant women. Supplement intakes, such as calcium (49.1% vs 52.8%), iron
(49.1% vs 52.8%) and folic acid (47.6% vs 60.3%) did not
differ among cases and controls.
There were no statistically significant differences
among the groups with regards to any of the micronutrients. We did not observe any statistically significant
association between household income and micro- or
macronutrient intake. There were no significant differences among the groups according to their ethnicity or
their place of origin (rural or urban).
Table 3 shows the results from the conditional
logistic regression that was performed in order to
determine which factors remain associated with PE
development. After the adjustment of the nutritional variables for gestational age, BMI and the difference between household income and household

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Nutritional status of Colombian women

Table 1 Clinical characteristics of patients

Age (years)
Gestational age (weeks)*
Primigravidae proportion*
Weight (Kg)*,**
Height (centimeters)
BMI (Kg/m2)*,**
Glycemia (mmol/L)*,**
Heart rate (b.p.m.)*,**
SBP (mm Hg)*,**
DBP (mm Hg)*,**
Total cholesterol (mmol/L)*,**
HDL (mmol/L)*,**
VLDL (mmol/L)*,**
LDL (mmol/L)*,**
Triglycerides (mmol/L)*,**

Cases
n = 201

Pregnant controls
n = 201

Non-pregnant controls
n = 201

26.45 7.22
34.09 4.21
36.87
71.10 13.42
158.94 6.49
27.92 5.01
4.47 1.2
84.81 13.46
151.08 14.39
95.50 9.49
6.35 1.71
1.39 0.4
1.58 0.56
3.37 1.50
3.44 1.22

26.71 7.21
37.69 3.47
25.89
68.06 10.82
158.83 13.33
26.68 3.83
4.08 1
79.19 8.81
112.64 6.72
68.66 6.31
6.87 1.58
1.51 0.35
1.47 0.49
3.89 1.52
3.19 1.07

26.73 7.06
NA
NA
59.08 10.92
159.04 7.81
23.41 4.68
4.61 0.64
77.30 9.11
104.12 10.37
69.54 7.79
5.16 1.20
1.34 0.32
0.75 0.3
3.07 1.06
1.63 0.66

*P < 0.001 between pre-eclamptic women and pregnant control women. **P < 0.001 between the three groups. Results expressed as
mean standard deviation. BMI, body mass index; DBP, diastolic blood pressure; HDL, high-density lipoprotein; LDL, low-density
lipoprotein; NA, not applicable; SBP, systolic blood pressure; VLDL, very-low-density lipoprotein.

Table 2 Energy and nutrient intake as estimated by food frequency questionnaire

Energy (K/cal)*,**
Proteins (gr)
Lipids (gr)
Carbohydrates (gr)*,**
Saturated fatty acids (gr)
Monounsaturated fatty acids (gr)
Fiber (gr)
Cereal*,**
Meet
Vegetables
Fruits*
Dairy*
Calcium (mg)
Iron (mg)
Potassium (mg)
Sodium (mg)
Vitamin C (mg)
Thiamin (mg)
Riboflavin (mg)
Niacin (mg)
Vitamin B6 (mg)
Dietary folate equivalent (mg)
Beta carotene (mg)
Retinol (mg)

Cases
n = 201

Pregnant controls
n = 201

Non-pregnant controls
n = 201

2430.17 767.40
89.30 28.62
66.35 25.43
387.15 125
23.50 9.80
22.96 9.35
29.24 11.08
4.46 1.85
1.43 0.67
6 2.62
2.59 1.82
347.11 272.95
439.21 344.48
15.53 5.10
5211.92 1706.83
3028.43 1149.09
299.26 139.45
1.79 0.58
2.64 0.92
23.17 7.30
2.77 0.90
508.32 173.22
9664.20 4838.27
392.03 187.45

2362.68 796.13
90.16 33.90
67.88 28.65
365.52 121.18
24.19 11.12
23.82 11.25
28.19 12.34
4.06 1.56
1.51 0.812
5.67 2.64
2.58 2
366.48 287.38
461.95 347.87
15.47 5.62
5075.68 1803.85
2886.13 1060.89
300.96 149.99
1.78 0.62
2.72 1.04
23.34 8.64
2.72 0.97
508.87 195.59
9062.37 4701.93
407.66 195.23

2212.85 805.94
84.48 34.26
64.15 29.45
339.91 123.94
22.28 10.68
22.92 11.02
26.42 12.07
3.86 1.54
1.49 0.79
6.03 3.13
1.89 1.36
299.09 274.38
383.06 325.53
14.58 5.75
4866.63 1906.57
2894.68 1339.32
281.28 144.87
1.68 0.65
2.49 0.99
22.90 8.64
2.59 0.98
472.67 199.19
9765.56 7754.75
338.37 174.97

*P < 0.001 between the three groups. **P < 0.001 between pre-eclamptic women and pregnant control women. Results expressed as
mean standard deviation.

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L. Reyes et al.

Table 3 Conditional logistic regression to determine

which factors are associated with pre-eclampsia
development
Variable

Odds ratio (95%

confidence interval)

Gestational age (weeks)

Body mass index (kg/m2)
Difference between
household income and
household expenditure
> than $US750
Carbohydrate intake
Fiber intake
Sodium intake > 2200 mg
Vitamin C intake > 200 mg

0.89 (0.830.95)
1.15 (1.061.25)
0.27 (0.090.81)

0.001
0.001
0.02

1.47 (1.042.08)
1.51 (1.052.18)
3.18 (1.198.48)
3.34 (1.288.74)

0.03
0.03
0.02
0.01

Micro and macronutrient intakes were adjusted by body mass

index, gestational age, and the difference between household
income and outcome.

expenditure, it was observed that carbohydrates,

sodium, vitamin C and fiber intake were associated
with PE development.

Discussion
We compared the nutritional status of women with PE,
healthy pregnant and non-pregnant women from six
urban settings in Colombia. Our results indicated that
women with PE had a lower gestational age, higher
heart rate and fasting blood glucose concentration as
well as a higher BMI compared to healthy pregnant
women. Regarding their nutritional status, women
with PE had higher carbohydrate and cereal intake
than healthy pregnant women. Also, results from the
conditional logistic regression showed that carbohydrate, fiber, sodium and vitamin C were associated
with the development of PE.
Even though it is recognized that maternal diet is one
of the main modifiable risk factors influencing pregnancy and childhood outcomes,23 the role of energy,
micro- and macronutrients in the development of PE is
debated. The discrepancies of findings between studies
may result from differing study designs; such differences include the use of different dietary assessment
methods and the time-point in pregnancy at which
food intake is measured.
In concordance with a previous report by Clausen
et al.,11 the consumption of energy and carbohydrates
was increased in women that developed PE. These
results support the proposed rapid nutritional transition experimented in Latin American populations.24 It
is recognized that socioeconomic factors, food avail-

502

ability and previous experiences regarding the sensory

properties of food, such as taste and texture, can influence what and how much is eaten.25 Urbanization and
socioeconomic transition have strong effects on food
availability and supply. Additionally, it has been
established that following this transition, there is an
increased consumption of refined foods, with a
decreased consumption of complex carbohydrates and
fiber24 as well as a marked preference for sweet and
salty foods and a decreased intake of fruits and vegetables. It has been shown that added sugars and fat
improves the taste of meals, thereby skewing food
choices. It is also known that preferences for fat
increased with bodyweight among obese women.26
Therefore, changes in food consumption could explain
the results from this study regarding carbohydrate and
sodium intake.
On the other hand, it is interesting to note that previous reports in Colombian pregnant women demonstrated an important association between nutritional
deficiencies (calcium, micronutrients, and fatty acids)
and PE.27 Nowadays, in a similar population, not only
was there no association between calcium and PE
development, but also, we found an association
between fiber and vitamin C consumption and PE
development. These findings could be attributed partly
to calcium supplementation; this is a preventive nutritional measure directed at overcoming a socioeconomic problem, which frequently impedes the access
to dairy products to poor women in societies from
developing countries during their pregnancy.28 Our
results regarding vitamin C and fiber must be interpreted carefully. Nutritional assessment of these
women was performed after the establishment of the
disease; therefore, either women with PE actually
increased their consumption of vitamin C and fiber
after its diagnosis to ameliorate the syndrome or an
introduction of a response bias could explain our
findings.
Moreover, it is well known that hypertriglyceridemia is associated with PE development.29
High-energy diets can lead to postprandial hypertriglyceridemia, which has been associated with monocyte
adhesion to the endothelial surface30 and increased oxidative stress by increasing the vascular superoxide
anion production and decreasing nitric oxide bioavailability.31 Therefore, a dyslipidemic background associated with a high-energy intake may affect the health
status of pregnant women and lead to PE. On the other
hand, Belo et al.32 demonstrated that as pregnancy
progresses and TG levels rise, there is a decrease in

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Nutritional status of Colombian women

LDL size, corresponding to an increased proportion of

atherogenic small dense LDL, which is more susceptible to oxidation.33 Interestingly, in our population
we found that women with PE had lower LDL levels
compared to healthy pregnant controls. We therefore
hypothesize that lower LDL concentrations in women
with PE are the result of increased LDL oxidation
rate; this may be caused by an increase in oxidative
stress, which subsequently will lead to endothelial
dysfunction.
The present study has some limitations. We used
FFQ to assess the nutritional status of participants and
although FFQ is the most frequently used method in
epidemiological studies34 it is not an appropriate
method for measuring absolute intake. Recall bias, and
lack of accuracy of the participants self-reported estimations of their habitual dietary intakes must be considered. The FFQ used, however, was previously
validated in our population in order to reduce the
impact of this bias.21 Due to the design of the study,
causality cannot be determined, only associations
between the exposure and the event can be formulated.
Although increased energy intake is required during
pregnancy, the increment is negligible in the first trimester and stands at only 350 kcal/d in the second and
500 kcal/d in the third trimester for women with a
normal BMI.35 Excessive energy intake during pregnancy results in increased fat deposition and a higher
BMI and augments the risk of PE, hypertension and a
preterm birth.36
Changes in diet style in Latin American countries are
having a negative impact on their populations health
status from a young age. Therefore, a disease such as
PE, which is associated with cardiovascular diseases in
the mother after its development37 and in her offspring,38 may be contributing to the cardiometabolic
epidemic in our population. Womens health polices
should aim for lifestyle modification before
pregnancy.39
In summary, results from the present study showed
that women with PE had higher energy, carbohydrates
and cereal intake compare to healthy pregnant controls, and that an increase in both carbohydrate and
sodium consumption were associated with the development of PE. The role of early detection and treatment
of unfavorable nutritional practices, such as an
increased carbohydrate or sodium intake, remains
unknown. They could be helpful, however, in reducing
excessive weight gain and reducing biochemical alterations of the lipid profile and carbohydrates related
to PE.

Acknowledgments
The authors acknowledge Colciencias (Departamento
Administrativo de Ciencia, Tecnologa e Innovacin)
for the financial support to the VILANO Group (Grant
N 6566-04-18061). The funding organization did not
have any role in the design and conduct of the study,
collection, management, analysis, and interpretation of
the data or the preparation, review, or approval of the
manuscript. All authors declare that there is no conflict
of interest with the subject of the manuscript. Authors
also wish to acknowledge Doctor Fredi Daz-Quijano
for his support with the statistical analysis.
Furthermore, the authors acknowledge the following institutions for their support: Clnica Materno
Infantil San Luis, Bucaramanga, Colombia; Hospital
Nio Jess, Barranquilla, Colombia; Clnica de la
Costa, Barranquilla, Colombia; Instituto del Corazn
de Santa Marta, Santa Marta, Colombia; ESE Hospital
Universitario Erasmo Meoz, Ccuta, Colombia; ESE
Hospital Manuel Uribe ngel, Envigado, Colombia;
and ESE Hospital San Juan de Dios, Floridablanca,
Colombia.

Disclosure
None declared.

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2012 The Authors

Journal of Obstetrics and Gynaecology Research 2012 Japan Society of Obstetrics and Gynecology