Clujul Medical 2013 V ol. 86 – no. 3MATERNAL OBESITY – A RISK FACTOR FOR METABOLIC SYNDROME IN CHILDREN MELINDA MOREA1, NICOLAE MIU1, VICENȚIU FLORIN… [623090]

259
Original Research
Clujul Medical 2013 V ol. 86 – no. 3MATERNAL OBESITY – A RISK FACTOR FOR METABOLIC
SYNDROME IN CHILDREN
MELINDA MOREA1, NICOLAE MIU1, VICENȚIU FLORIN MOREA2,
RODICA CORNEAN1
1Pediatric Emergency County Hospital Cluj-Napoca, Iuliu Hațieganu University
of Medicine and Pharmacy, Cluj-Napoca, Romania
2Emergency County Hospital Cluj-Napoca, Romania
Abstract
Objective. To determine the association between the metabolic syndrome in
children (MS) and the pre-pregnancy nutritional status of the mother.
Design and methods. A total number of 180 children aged between 6-19 years
were examined. Self reported data about parents and their children were collected. The
children underwent physical examination; weight, height, waist circumference, blood
pressure (BP) were measured. The nutritional status of the children was assessed by
body mass index (BMI) and laboratory tests needed to diagnose MS were performed.
IDF criteria for MS were used in children 10 years and older, and age and gender
specific cut-off points in children younger than 10 years. The mothers were classified
in the normal weight, overweight and obese categories according to the pre-pregnancy
BMI. The statistical analysis of the data was descriptive and inferential analysis. In the
bivariate analysis of the association between qualitative variables, we used the Chi-
Square test and the exact Fisher test. The statistical analysis was performed with SPSS
v 13.0.
Results. 73 (40.55%) children were normal weight, 54 (30%) were overweight
and 53 (29.44%) were obese. None of the normal weight children, 16 (29.60%) of the
overweight and 23 (43.40%) of the obese ones had MS; 125 (69.44%) of the mothers
were normal weight, 44 (24.44%) were overweight and 11 (6.11%) were obese.
Pre-pregnancy maternal BMI was significantly associated with offspring MS in
both genders, obese children and in the 10-16 age group.
Conclusions. Pre-pregnancy maternal overweight/obesity represents a risk
factor for offspring MS. The results are very difficult to compare between studies
because of different cut-off values and definition of MS in children. If prevention is the
goal rather than treatment, the perinatal period may be an important focus for future
research.
Keywords: obesity, overweight, metabolic X syndrome, child, fetal
programming, risk factors .
Manuscript received: 21.01.2013
Received in revised form: 29.05.2013
Accepted: 31.05.2013
Address for correspondence: [anonimizat]
Obesity and its related diseases represent a threat
for the population health and lifestyle, considering the
increased prevalence of the disease in the last decades.
The prevalence of obesity among women of child-
bearing age is increasing, in the USA 34% are obese
and 59.5% overweight. In Europe the prevalence ranges
between 6.2% – 36.5% with geographical variations, higher in Central, Eastern and Southern Europe than in Western
and Northern Europe [1,2].
This increase is the result of several factors, lifestyle
playing an important role. Emerging and increasing
evidence suggest the role of factors acting early in the
life of the individual and their long term influence on
the metabolism, therefore pregnancy represents a critical
period. One of these factors is the maternal overweight/
obesity.
Recent studies on animals suggest the alteration of
the oocytes quality, the influence of maternal obesity on
the conception product being previous to fertilization. The

260
Pediatrics
Clujul Medical 2013 V ol. 86 – no. 3obesity risk in offsprings of females with weight excess
at the time of conception is maintained even if the diet is
normal during pregnancy. Several modifications of the body
composition occur, such as the increase in intramuscular
fat content and altered expression of genes important
in muscle growth and metabolism, leading to insulin-
resistance. The maternal obesity influences the appetite,
the physical activity, the structure and the function of the
muscular tissue, as well as the alteration of adipocytes
biology on a long-term basis [3].
An association between the obesity of the child and
the BMI of the mother before and during pregnancy may
be observed in humans, too. Alterations were observed in
the newborn body composition if the mother had weight
excess, such as an increase of the quantity and percentage
of fat tissue. It seems that these associations are maintained
into adulthood [3].
The increase of fatty tissue and the weight of the
newborns from obese mothers are the result of metabolic
changes during pregnancy (decrease of insulin sensitivity,
increase of insulin resistance), as opposed to normal weight
women, thus affecting the foetus-placenta development
and growth [4].
Boney and co., studying a group of children of
mothers with gestational diabetes and a group of children
of mothers without gestational diabetes, found the same
association between the maternal obesity and MS in
children, the odds of MS being twice greater in children
with obese mothers [5]. This would suggest that the
foetal hyperinsulinemia in foetuses of overweight/obese
mothers without gestational diabetes, is due to maternal
hyperglycaemia, but with values below the threshold for
the diagnosis of gestational diabetes. There is a relation
between high BMI of the mother and hyperinsulinemia
of the developing child (showed via determination of the
C peptide from the umbilical cord) [6]. The high insulin
secretion in offsprings of overweight/obese women is
maintained during the entire life of the child [5].
Changes of the fat and protein metabolism may be noticed along the glucose metabolism changes, especially
in the case of excessive alimentary intake of the mother.
Increased serum glucose levels of the mother, free fatty
acids and amino acids produce permanent alterations in
the regulation of the appetite, the neuronal and endocrine
systems and the energetic metabolism of the foetus, thus
determining obesity and a high risk of metabolic syndrome
in the subsequent life of the individual [7].
Studies have evidenced metabolism disturbances
in obese women during pregnancy and support Baker and
Gluckman’s hypothesis arguing the “foetal origins” of the
diseases, subsequently named the “Developmental Origins
of Adult Health and Disease” (DOHaD). Therefore one may
assume that the influence the maternal obesity on the child
starts during intrauterine life and continues throughout the
life of the individual [4,8,9].
Objective of the Study
To determine the association between metabolic
syndrome in children and the pre-pregnancy nutritional
status of the mother.
Design and methods
We performed a cross sectional retrospective study in
a group of 180 subjects, children aged between 6-19 years
old, referred to the Paediatric Clinic 2 of Cluj-Napoca, and
children from 2 schools in the same city. The study was
performed during the period 2005-2010. The parents of
the children gave their informed consent to use the data in
this study. We obtained the approval of the medical ethics
committee of the Pediatric Emergency County Hospital.
Data on the parents and maternal anthropometric
data at the time of conception (pre-pregnancy nutritional
status) were obtained by anamnesis. The children were
measured: weight, height, waist circumference (WC) and
blood pressure (BP). We calculated the body mass index
(BMI) for the children and the mothers
The laboratory tests performed were: fasting glucose
level, oral glucose tolerance test, fasting insulin level, total
Table I. Metabolic syndrome in children-definition criteria.
Age WC TG HDL BP Glucose
<10 years >p90>p90
and/or
≥150 mg/dl<p10
and/or
<40 mg/dl>p90gl ≥100 mg/dl
and/or
OGTT ≥200 mg/dl
and/or
HOMA-IR >2.5
10-16 years >p90 ≥150 mg/dl <40 mg/dlBPs ≥130 mmHg
BPd ≥85 mmHggl ≥100 mg/dl
and/or
OGTT ≥200 mg/dl
and/or
HOMA-IR >2.5
>16 yearsGirls ≥80 cm
Boys ≥94 cm≥150 mg/dlGirls <50 mg/dl
Boys <40 mg/dlBPs ≥130 mmHg
BPd ≥85 mmHggl ≥100 mg/dl
WC: waist circumference; HDL: high-density lipoprotein cholesterol; BP: blood pressure BPs systolic BPd diastolic;
gl: fasting glucose; OGTT: oral glucose tolerance test.

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Original Research
Clujul Medical 2013 V ol. 86 – no. 3cholesterol, HDL cholesterol, triglycerides.
We defined the metabolic syndrome according to
IDF criteria for children and adolescents [10]. Considering
there is no clear definition of this syndrome in children
younger than 10 years old, we used age and gender specific
cut-off points, as mentioned in the table, according to
each variable [11-15]. The definition used in this study is
presented in the table I. We considered a MS diagnosis if
at least 3 of 5 criteria were present, based on the latest IDF
recommendations in adults [16].
Subjects were distributed into 3 age groups (youn-
ger than 10 years, between 10-16 years old and older than
16 years) according to the MS definition in children, into
two groups by gender and into 3 groups according to the
nutritional status. The nutritional status of the children
was assessed based on the BMI and the groups of normal
weight, overweight and obese children according to the
IOTF references were established [17]. The children were
also grouped depending on the pre-pregnancy nutritional
status of the mother, BMI: <25 kg/m2 normal weight,
between 25-29.99 kg/m2 overweight, ≥30 kg/m2 obese.
Only those with idiopathic obesity were included in this
study, we excluded the mothers and children with obesity
due to other causes and children with diseases which might
influence the laboratory tests.
Statistical method
The statistical analysis of the data was descriptive
and inferential analysis. In the bivariate analysis of the
association between qualitative variables, we used the Chi-
Square test and the exact Fisher test. The quantification of the association was estimated by the odds ratio (OR) and
the 95% confidence interval. The significance level for all
tests was α=0.05. Thus, the type 1 error rate we are willing
to assume is 5%. Test significance is given by the bilaterally
observed significance level, p<0.05. The exact Fisher test
was used if at least 20% of the theoretical frequencies were
less than 5. The statistical analysis was performed with
SPSS v 13.0.
Results
Of the 180 subjects, 98 (54.44%) were girls, 82
(45.55%) were boys. There were 78 (43.33%) under 10
years old, 90 (50%) between 10-16 years old, and 12
(6.66%) older than 16 years. According to the nutritional
status of the children, we had 73 (40.55%) normal weight,
54 (30%) overweight and 53 (29.44%) obese (table II).
By analyzing the association between the pre-
pregnancy nutritional status of the mother and the presence
of the metabolic syndrome in children we noticed an
increasing percentage of children with MS with increasing
pre-pregnancy maternal BMI. A percentage of 12.8% of
children with normal weight mothers (BMI <25 kg/m2) had
MS, the percentage increased to 38.6% in children with
overweight mothers (BMI 25-29.99kg/m2) and reached
54.4% in children whose mothers were obese (BMI ≥30
kg/m2) at the time of conception. We found a statistically
significant association between the pre-pregnancy
nutritional status of the mother and the presence of MS in
children (Chi-Square test, p<0.001) (table III).
Table II. Gender, age and nutritional status of the children.
Gender Age Nutritional status
Girls
Boys98 (54.44%)
82 (45.55%)< 10 years 78 (43.33%) Normal weight 73 (40.55%)
10-16 years 90 (50%) Overweight 54 (30%)
>16 years 12 (6.66%) Obese 53 (29.44%)
Table III. Metabolic syndrome in children with overweight, obese and normal weight mothers.
pre-pregnancy BMI of the motherMSTotal Pearson Chi-Squarepresent absent
≥30number of subjects 6 5 11 χ2=20.262
% 54.5% 45.5% 100.0% df=2
25 <30Number of subjects 17 27 44 p<0.001
% 38.6% 61.4% 100.0%
<25Number of subjects 16 109 125
% 12.8% 87.2% 100.0%
Total Number of subjects 39 141 180
1 cells (16.7%) have expected count less than 5. The minimum expected count is 2.38.
Table IV . Metabolic syndrome in children with overweight/obese and normal weight mothers.
pre-pregnancy BMI of the motherMSTotal Pearson Chi-Squarepresent absent
≥25Number of subjects 23 32 55 χ2=18.950
% 41.8% 58.2% 100.0% df=1
<25Number of subjects 16 109 125 p<0.001
% 12.8% 87.2% 100.0% OR=4.89
Total Number of subjects 39 141 180 95%CI=2.313-10.365

262
Pediatrics
Clujul Medical 2013 V ol. 86 – no. 3A percentage of 41.8% of children with overweight
or obese mothers at the time of conception had MS as
opposed to 12.8% of children whose mothers were of
normal weight at the time of conception. The relation was
statistically significant p<0.001. The odds of having MS
was 4.89 times higher in children whose mothers were
overweight or obese at the time of conception (table IV).
The association between the pre-pregnancy nutri-
tional status of the mother remained statistically significant
analyzed by gender: 42.3% of the girls from overweight
or obese mothers had MS versus 11.1% of the girls with
normal weight mothers at the time of conception. For
boys, the percentages were similar: 41.4% and 15.1%
respectively.
The study on the association between pre-pregnancy
nutritional status of the mother and MS in children was
performed in the sub-groups of overweight and obese
children; in the sub-group of normal weight children we
had no subjects with MS (table V).
Among the overweight children having MS, 33.3%
had overweight or obese mothers and 28.6% had mothers
with normal weight. For the obese children we found a
statistically significant association between the BMI of the mother at the time of conception and MS presence in
children (p<0.05). A percentage of 55.9% of the obese
children with overweight or obese mothers at the time
of conception had MS versus only 21.1% of those with
normal weight mothers. The odds of having MS in obese
children with overweight/obese mothers with at the time
of conception is of 4.75 (95%CI=1.302-17.327) (table VI).
In the analysis of the relation between the nutritional
status of the mother at the time of conception and the
presence of MS in children, in the 3 age groups, we observed
increased percentages of MS in children from overweight
or obese mothers versus those from normal weight mothers
for all 3 age groups. The relation was statistically significant
only for the 10-16 years age group. For this age group, a
percentage of 48.0% of those with overweight or obese
mothers presented MS versus 10.8% of those with normal
weight mother at the time of conception (table VII).
Discussion
The weight gain and the metabolic changes during
childhood are the result of the interaction of various
factors, including the genetic predispositions and the
lifestyle (alimentation, physical activity) that developing
Table V . Metabolic syndrome in girls and boys with overweight/obese and normal weight mothers.
Girls
pre-pregnancy BMI of the motherMSTotal Pearson Chi-Squarepresent absent
≥25Number of subjects 11 15 26 χ2=11.895
% 42.3% 57.7% 100.0% df=1
<25Number of subjects 8 64 72 p<0.001
% 11.1% 88.9% 100.0% OR=5.86
Total Number of subjects 19 79 98 95%CI=2.012-17.109
Boys
pre-pregnancy BMI of the motherMSTotal Pearson Chi-Squarepresent absent
≥25Number of subjects 12 17 29 χ2=7.022
% 41.4% 58.6% 100.0% df=1
<25Number of subjects 8 45 53 p=0.014
% 15.1% 84.9% 100.0% OR=3.97
Total Number of subjects 20 62 82 95%CI=1.383-11.396
Table VI. Metabolic syndrome in overweight and obese children with overweight/obese mothers.
Overweight
pre-pregnancy BMI of the motherMSTotal Fisher’s Exact Testpresent absent
≥25Number of subjects 4 8 12 p=0.734
% 33.3% 66.7% 100.0%
<25Number of subjects 12 30 42
% 28.6% 71.4% 100.0%
Total Number of subjects16
29.60%38 54
Obese
pre-pregnancy BMI of the motherMSTotal Pearson Chi-Squarepresent absent
≥25Number of subjects 19 15 34 χ2=6.019
% 55.9% 44.1% 100.0% df=1
<25Number of subjects 4 15 19 p=0.021
% 21.1% 78.9% 100.0% OR=4.75
Total
Number of subjects23
43.40%30 5395%CI=1.302-17.3027
Overweight and obese39
36.45%68 107
2 cells (33.3%) have expected count less than 5. The minimum expected count is 3.04.

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Original Research
Clujul Medical 2013 V ol. 86 – no. 3early during the childhood [18]. The family is one of the
most important components influencing the metabolic risk
factors in children. The studies of the genetic-lifestyle
interaction demonstrated the capacity of the environment
to influence the genetic predisposition [19].
The prevalence of the metabolic syndrome in our
study was high, 43.3% in obese children and 36.45% in
obese and overweight children, within the range of other
studies using IDF definition (16.4%-44.2%); in Europe the
median prevalence was 21% with range between 8.9%-50%
[20]. Studies in our country using IDF definition revealed
a prevalence of metabolic syndrome in obese children
between 20% [21] and 58% [22]. The high prevalence and
variations in the prevalence may be due to the small sample
size.
In our study, the BMI of the mother was significantly
associated with the MS of the child, with the percentage
of those with MS proportional with overweight/obesity
of the mother at the time of conception. The odds of
MS in children increased almost fivefold for those with
overweight or obese mothers. The significant association
is consistent with the literature, but the percentage of those
with MS in our study was up to four times higher (Hirschler
8.5% vs 41.8%), and the odds of developing MS double
(OR: Boney 1.8 Ekelund 1.61 vs 4.89). This might be
explained by the various definitions of MS used, the age of
the subjects included in the study, the obesity type of the
mother [5,23,24].
Hirschler, in his initial studies, found a significant
correlation between maternal abdominal-type obesity
(assessed by WC) and MS in children, even stronger than
with the metabolic risk factors, including MS of the mother.
The subsequent studies which included 5 anthropometrical
indices of the mother do not show any significant differences between their capacity to identify children with MS or
overweight risk, the best association being the relation with
the waist circumference of the mother. Pre-pregnancy BMI
cut-off value which predicts the metabolic syndrome in
children, as result of this study, was suggested as 30 kg/m2,
within the range of 27-30 kg/m2 for optimal specificity and
sensibility [18,23].
The effect of intrauterine conditions on the foetus
seems to extend throughout the entire life of the individual,
by affecting the body composition, the insulin secretion,
the insulin resistance, but also the appetite and the lifestyle
via the central nervous system by several mechanisms
demonstrated only in animal models [3,5]. In our study,
we found a significant association between the overweight/
obesity of the mother and the MS of the child only within
the 10-16 years age group where we used the recommended
non-modified IDF definition for this age group. Ekelund
found an increase of the odds of developing MS at the age
of 15 of 1.36 times higher than at the age of 10.
The association of the overweight/obesity of the
mother with the MS of the child was significant in both
genders, with close percentages of the girls and boys with
MS and having overweight/obese mothers, similar with
other results in literature [5]. However the odds of having
MS in girls was higher than in boys (5.86 vs. 3.97) in our
study, as opposed to the results obtained by Ekelund, where
the boys odds was 2.63 times higher than girls (the study
was performed in children with obese and normal weight
mothers).
The significant association between the overweight/
obesity of the mother and the presence of MS only in obese
children, considering that we had no normal weight children
with MS, raises questions regarding the existence of the
relationship between the overweight of the mother and the Table VII. Metabolic syndrome in three age group children with overweight/obese mothers.
<10 years
prepregnancy BMI of the motherMSTotal Fisher’s Exact Testpresent absent
≥25Number of subjects 7 17 24 p=0.211
% 29.2% 70.8% 100.0%
<25Number of subjects 8 46 54
% 14.8% 85.2% 100.0%
Total Number of subjects 15 63 78
1 cells (25.0%) have expected count less than 5. The minimum expected count is 4.62.
10-16years
prepregnancy BMI of the motherMSTotal Pearson Chi-Squarepresent absent
≥25Number of subjects 12 13 25 χ2=15.028
% 48.0% 52.0% 100.0% df=1
<25Number of subjects 7 58 65 p<0.001
% 10.8% 89.2% 100.0% OR=7.64
Total Number of subjects 19 71 90 95%CI=2.522-23.192
> 16 years
prepregnancy BMI of the motherMSTotal Fisher’s Exact Testpresent absent
≥25Number of subjects 4 2 6 p=0.242
% 66.7% 33.3% 100.0%
<25Number of subjects 1 5 6
% 16.7% 83.3% 100.0%
Total Number of subjects 5 7 12

264
Pediatrics
Clujul Medical 2013 V ol. 86 – no. 3MS of the children, or whether there is just a link between
MS and child’s obesity. Considering the small percentage
of normal weight children with MS, the relatively small
number of the group can limit the results.
Significant differences between the BMI of chil-
dren with MS and children without MS and the BMI of
the mother were also highlighted by the European Youth
Hearth Study. Although the maternal BMI was significantly
and independently associated with the MS of the child
and BMI, the same relationship was not found in respect
to the metabolic components of the MS. Therefore it could
be argued that the adiposity of the mother determines the
MS of the child via his adiposity, considering the well
known association between the obesity of the mother and
the increased weight at birth and further obesity of the
child. The difference as compared to our study is the MS
definition used, the central-type obesity being a sine qua
non condition for the MS definition.(24) The weight of the
mother before the pregnancy was determined by anamnesis,
which might have influenced the accuracy of the data,
given the time lapsed since the childbirth. Therefore a
prospective study could bring more data.
The conclusions of this study are limited by its
cross sectional design. Due to the small sample size, the
statistical significance of the prevalence of MS in our study
was limited. It shows the association between the MS of
the child and the risk factors, but it cannot directly predict
subsequent complications.
Conclusions
The overweight/obesity of the mother represents
a risk factor for the metabolic syndrome of the child,
especially in obese children. Further studies are needed
in order to clarify the way in which the weight excess of
the mother influences the development of the metabolic
syndrome in children, directly or via the obesity of the child.
Both genders are similarly affected by the overweight/
obesity of the mother.
Considering the studies design differences, the
population differences, the lack of a unanimously accepted
definition of the metabolic syndrome of the child, the
studies using different definitions, the various cut-off
values of metabolic syndrome elements, the results are
difficult to compare.
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