European Journal of Pediatrics

https://doi.org/10.1007/s00431-018-3109-y

ORIGINAL ARTICLE

Sociocultural risk factors for developmental delay in children aged

3–60 months: a nested case-control study
Aylin Demirci 1 & Mehtap Kartal 2

Received: 18 August 2017 / Revised: 2 January 2018 / Accepted: 28 January 2018

# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Identifying children at risk for developmental delay (DD) is important for improving prognosis. In this sense, we estimated
sociocultural factors that may be associated with DD in early childhood. In our nested case-control study, 95 were included in the
case group and 190 were randomly selected to control group. To identify the risk factors, we conducted a backward conditional
logistic regression and a final multivariable model was developed. Maternal age of ≥35 years, low maternal and paternal
education level, low socioeconomic level, consanguineous marriage, and delivery by cesarean section increased the risk of
DD. After adjustment, the risk of DD was significantly increased by maternal age ≥ 35 years (odds ratio (OR) 3.04, 95%CI
1.38–6.70), maternal education level of primary school or lower (OR 14.56, 95%CI 5.40–39.24), consanguineous marriage (OR
3.99, 95%CI 1.69–9.40), and delivery by cesarean section (OR 3.34, 95%CI 1.80–6.18).
Conclusion: DD can be identified early during well-child visits. In such cases, it is critical for the health of the child and
community to screen for possible risk factors, eliminate the causes, and refer families to rehabilitation services.

What is known:
• The causes of DD may be classified into prenatal, perinatal, and postnatal factors.
• Early identification may improve later outcomes of DD. Most studies conducted on this topic have focused on prematurity.
What is new:
• This study focused on maternal, paternal, and sociocultural factors that may be associated with DD in early childhood in this study that was conducted
on a community-based sample.
• The risk of DD was increased by maternal age ≥ 35 years, maternal education level of primary school or lower, consanguineous marriage and delivery
by cesarean section.

Keywords Developmental delay . Ages and Stages Questionnaires . Risk factors . Child

Abbreviations OR Odds ratio

ASQ-TR Ages and Stages Questionnaire-Turkish Version PHC Primary healthcare centers
CI Confidence interval
DD Developmental delay

Introduction
Communicated by: Mario Bianchetti
Developmental delay (DD) is defined as delays in areas of
* Aylin Demirci speech and language development, motor development, social
aylin_akdemir@hotmail.com development, and cognitive development [14]. Although the
estimated prevalence of DD is generally 5–15% in the pediat-
Mehtap Kartal
mehtap.kartal@deu.edu.tr
ric population [20], the reported prevalence varies depending
on the socioeconomic characteristics of the study population,
1
Bayrakli District Directorate of Health, 1606/1 Street, Apt. 10, case definition, and age range [6].
Bayrakli, 35530 Izmir, Turkey Identifying children at risk for DD in the first year of life
2
Department of Family Medicine, Dokuz Eylul University School of and initiating rehabilitation early are important for improving
Medicine, Inciralti, Izmir, Turkey prognosis. In this sense, it is essential to determine the

etiological factors of DD in order to manage the problem in
early childhood [19]. Biological and psychosocial risk fac-
tors affecting child development are more prevalent in
developing countries in particular [8], and more than
200 million children under the age of 5 years are unable
to complete their development normally in these countries
[7].
The causes of DD may be classified into prenatal,
perinatal, and postnatal factors. In addition, brain func-
tion is associated with a number of risk factors, includ-
ing biological, environmental, and social factors. Many
of these factors may be preventable or modifiable, and
thus, their early identification may significantly improve
later outcomes of DD [7].
Based on the current evidence concerning DD, devel-
opmental screening of children at specific intervals is rec-
ommended in order to reverse long-term effects [21].
During these screens, it is important to identify situations
which may be risk factors for DD. Most studies conducted
on this topic have been hospital-based and have focused
on low birth weight or preterm children. Few studies have
been conducted on community-based samples.
The aim of our study was to estimate maternal, pa-
ternal, and sociocultural factors that may be associated
with DD in early childhood, such as maternal gestation-
al age, maternal and paternal educational status, socio-
economic status of family, consanguineous marriage,
and delivery type. Furthering our knowledge on this
subject may help both obstetricians and family physi-
cians optimize antenatal obstetric care, as well as facil-
itate the identification of children who may have an
increased risk of DD in early childhood.
Materials and methods
Participants
This nested case-control study is part of a cross-sectional
study on the prevalence of DD [3]. In a community-based
cohort of 160,446 children, 1514 children aged 3–
60 months were sampled and the Turkish version of the
second edition of the Ages and Stages Questionnaires
(ASQ-TR) were administered to all. The development of
children whose scores were lower than the cut-off score in
two or more developmental areas was regarded as
Bdelayed,^ while the development of children who obtain-
ed scores higher than the cut-off score in five developmen-
tal areas was regarded as Bnormal^ (8). Of these 1514 chil-
dren, 95 were determined as delayed and constituted the
case group after the assessment with the questionnaire. As
there could be at most two children as controls for each
case that could be matched on age and sex, 190 were
Eur J Pediatr
randomly selected among 1419 children whose develop-
ment was regarded as Bnormal.^
Procedure
A questionnaire prepared by the researcher and the ASQ-TR
where applied to mothers on a voluntary basis via face-to-face
interview in an environment in which the child and the mother
felt comfortable allocating sufficient time. The questionnaire
prepared by the researcher contains questions about maternal
gestational age, maternal/paternal education, paternal occupa-
tion, consanguineous marriage, prenatal and perinatal charac-
teristics, type of delivery, prematurity, and child birth order.
The classification developed by Neyzi et al. was used to de-
termine the socioeconomic level of the participating families
[13]. According to this classification, the highest socioeco-
nomic level is 1 and the lowest level is 4, depending on pa-
ternal occupation and maternal and paternal education level.
Measures
ASQ-TR and assessment
The ASQ, developed by Bricker et al., was used to evaluate
the developmental status of the children [1]. Kapci et al.
assessed the validity and reliability of the Turkish version of
the second edition of the questionnaire and determined its
sensitivity to be 94.0% and its specificity to be 85.0%. The
ASQ has different question forms for 19 different age ranges
from 4 to 60 months. The ASQ-TR can be clearly understood
and easily completed by parents, caregivers other than parents,
and teachers who know the child [8]. When the mothers were
sure that their children were able to achieve the skills referred
to in an item on the form, that item was marked. If they were
not sure whether the child was able to achieve a skill stated in
an item or if that skill was not observed by the mother, mark-
ing was completed after asking the child to perform that skill.
The development of children whose scores were lower than
the cut-off score in two or more developmental areas was
regarded as Bdelayed,^ while the development of children
who obtained scores higher than the cut-off score in five de-
velopmental areas was regarded as Bnormal.^ For children
who obtained scores lower than the cut-off score in only one
area, development was accepted as Bnormal,^ but their
families/primary care physicians were informed that their de-
velopment should be monitored in the following months [8].
Statistical analysis
Statistical analyses were performed using the SPSS software
version 15.0 (Data Processing Unit at Dokuz Eylul University
in Izmir, Turkey). Categorical variables were expressed as
frequency and percentage distributions. The univariable
Eur J Pediatr
analyses to identify variables associated with DD were inves-
tigated using the chi-square test. To identify the risk factors of
DD, we conducted a backward conditional logistic regression,
and a final multivariable model was developed where risk
factors < 0.05 were included to estimate the odds ratio (OR)
and 95% confidence intervals (CI). Risk factors included in
the full model were maternal gestational age (< 35 years vs. ≥
35 years), maternal education (primary school and lower vs.
others), paternal education (primary school and lower vs.
others), socioeconomic level of the family (Level 4 vs. others),
consanguineous marriage (yes vs. no), and type of delivery
(cesarean vs. vaginal). Power analysis showed that the vari-
ables that were included in the final model (Table 4) had a
power that changes between 94.45% (for gestational age) and
100% (for maternal education) which was evaluated as suffi-
ciently accurate for the purpose of this study.
Results
A total of 285 children between 3 and 60 months of age were
included in the study, 95 in the case group and 190 in the
control group. The case and control groups comprised
56.8% males and 43.2% females. The distributions of the
study subjects by sex and age group are shown in Table 1.
Significant associations were observed between DD and
maternal age at pregnancy, maternal and paternal education
level, family socioeconomic level, and consanguineous mar-
riage (Table 2).
The children of mothers who did not take iron and folate
supplementation had significantly higher rates of DD
(Table 3). In terms of the child’s health and delivery, the prev-
alence of DD was significantly higher among cases who had a
history of neonatal jaundice and among children who have
two or more siblings. The rate of DD was even higher among
children delivered by cesarean section (Table 3).
Table 1 Distribution of
developmental delay status of Developmental delay
children according to gender and (n = 95)
age
n %
Gender
Male 54
Female 41
Age groups (months)
3–12 20
13–24 34
25–36 19
37–48 12
49–60 10
Maternal age of ≥ 35 years, low maternal and paternal ed-
ucation level, low socioeconomic level, consanguineous mar-
riage, and delivery by cesarean section increased the risk of
DD. After adjustment for paternal education level and socio-
economic level of the family, the risk of DD was significantly
increased by maternal age ≥ 35 years (OR 3.04, 95%CI 1.38–
6.70), maternal education level of primary school or lower
(OR 14.56, 95%CI 5.40–39.24), consanguineous marriage
(OR 3.99, 95%CI 1.69–9.40), and delivery by cesarean sec-
tion (OR 3.34, 95%CI 1.80–6.18) (Table 4).
Discussion
Normal early childhood development is not only important in
childhood, but impacts success and well-being throughout
life. Problems arising in early childhood development may
be a major cause of morbidity and mortality in adulthood.
For this reason, monitoring development starting in child-
hood, identifying possible problems, and preventing or halting
their progression can improve affected individuals’ quality of
life. Systematic and professional child monitoring is an abso-
lute requirement for fulfilling these objectives [21].
Knowing the risk factors that can lead to DD in early child-
hood will greatly facilitate clinicians in effective monitoring.
In the present study, we investigated sociocultural factors be-
lieved to lead to early childhood DD. Previous studies con-
ducted in Turkey on this topic were conducted primarily in
high-risk children (e.g., low birth weight neonates, those treat-
ed in intensive care). In this respect, our study is unique be-
cause it included case and control groups selected from a
large, community-based sample.
We observed that DD was significantly associated with ma-
ternal age of ≥ 35 during pregnancy (p < 0.001), low maternal
and paternal education level (p < 0.001), consanguineous mar-
riage (p < 0.001), low family socioeconomic status (p = 0.004),
No developmental delay
(n = 190)
n % p
1.000
56.8 108 56.8
43.2 82 43.2
1.000
21.1 40 21.1
35.8 68 35.8
20.0 38 20.0
24.6 24 12.6
10.5 20 10.5
 Eur J Pediatr

Table 2 Sociodemographic
profile of cases (developmental Cases Controls
delay) and controls (n = 95) (n = 190)

n % n % x2 p

Maternal gestational age (years) 15.095 < 0.001

< 35 67 70.5 169 88.9
≥ 35 28 29.5 21 11.1
Maternal education 37.956 < 0.001
Primary school and lower 62 65.3 60 31.6
Secondary school 27 28.4 63 33.2
High school and university 6 6.3 67 35.3
Paternal education 28.931 < 0.001
Primary school and lower 48 50.5 57 30.0
Secondary school 38 40.0 57 30.0
High school and university 9 9.5 76 40.0
Socioeconomic level of family 13.301 0.004
1 6 6.3 35 18.4
2 11 11.6 33 17.4
3 29 30.5 59 31.1
4 49 51.6 63 33.2
Consanguineous marriage 20.455 < 0.001
No 72 75.8 179 94.2
Yes 23 24.2 11 5.8

lack of iron supplementation during pregnancy (p = parental education level and family socioeconomic level
0.023), delivery by cesarean section (p < 0.001), neona- were not associated with DD.
tal jaundice at levels requiring treatment (p < 0.001), and We found that a maternal age of 35 years or older at the
birth order (p < 0.001). In our multivariable model, time of pregnancy increased the risk of DD. There are studies

Table 3 Risk factors for

developmental delay among cases Cases (n = 95) Controls (n = 190)
and controls
n % n % x2 p

Hypertension during pregnancy 12 12.6 4 2.1 13.243 0.001

Diabetes during pregnancy 18 18.9 3 1.6 27.991 0.001
Iron supplement use during 79 83.2 176 92.6 6.035 0.023
pregnancy
Folic acid supplement use 88 92.6 187 98.4 6.270 0.018
during pregnancy
Smoking during pregnancy 7 7.4 4 2.1 4.728 0.046
Preterm 14 14.7 4 2.1 17.079 < 0.001
Mode of delivery 13.440 < 0.001
Vaginal 42 44.2 127 66.8
Cesarean 53 55.8 63 33.2
Hypoxia at birth 9 9.5 1 0.5 14.975 < 0.001
Birth weight (gr) 20.971 < 0.001
< 2500 13 13.7 2 1.1
2500–4000 80 84.2 186 97.9
≥ 4000 2 2.1 2 1.1
Jaundice 83 87.4 45 23.7 103.819 < 0.001
Respiratory distress 26 27,4 1 0.5 53.207 < 0.001
Birth order 15.479 < 0.001
First 29 30.5 65 34.2
Second 30 31.6 92 48.4
Third or above 36 37.9 33 17.4
Eur J Pediatr
Table 4 Multivariate analysis for risk factors of developmental delay
Unadjusted
B S.E.
Maternal gestational age (≥ 35 yrs) 1.21 0.32
Maternal education
Primary school and lower 2.45 0.46
Secondary school 1.57 0.48
High school and university
Consanguineous marriage 1.65 0.39
Type of delivery (Cesarean) 0.93 0.26
a
Adjusted for paternal education, socioeconomic level of family
in the literature demonstrating a link between maternal age
and complications during pregnancy [4, 16]. Pregnant women
over the age of 35 are at higher risk of miscarriage, fetal
chromosomal and congenital anomalies, gestational diabetes,
placenta previa, delivery by cesarean section, and hyperten-
sion [2]. Increase in maternal age has been associated with
increases in comorbidities and obstetric complications, and
an especially sharp rise in the rate of cesarean delivery has
been noted in women over 35 years of age [22].
In our multivariable model, we found a significant asso-
ciation between Cesarean birth and developmental delay.
Kerstjens et al. observed a significant link between DD
and cesarean delivery in a univariable model (OR 1.81,
95%CI 1.08–3.03), but this relationship was not significant
in multivariable models based on socioeconomic status and
parity (OR 1.42, 95%CI 0.72–2.78) [9]. However, consid-
ering that cesarean delivery is preferred for high-risk preg-
nancies and conditions that negatively impact the health of
the fetus, it can be supposed that the factors leading to these
conditions may also lead to DD. In addition, a cesarean
section is a major operation, and the intraoperative risks it
entails may also contribute to this significance.
We found that maternal education level of primary
school or lower increased the risk of DD by 14.56-fold
(95%CI 5.40–39.24). Paternal education level and family
socioeconomic status were not associated with DD in
multivariable analysis. Several studies have demonstrated
that maternal/paternal education level, family structure,
and family socioeconomic level significantly affect devel-
opment [10, 17, 18]. In fact, Vohr et al. argued that high
socioeconomic status may positively impact development
by changing the course of problems related to preterm
birth [24]. In a study of children 2–5 years old who ex-
hibited signs of autistic behavior, Mukaddes et al. deter-
mined that these children had been neglected by their
mothers from an early age and that their families had been
devoid of social contact [12]. Epir et al. also observed that
Adjusteda
OR(95%CI) B S.E. OR(95%CI)
p p
3.36 (1.79–6.33) < 0.001 1.11 0.40 3.04(1.38–6.70) 0.006
11.54(4.66–28.56) < 0.001 2.68 0.51 14.56(5.40–39.24) < 0.001
4.79(1.85–12.36) < 0.001 2.05 0.53 7.74(2.77–21.68) < 0.001
1.00 (reference) 1.00 (reference)
5.20(2.41–11.21) < 0.001 1.38 0.44 3.99(1.69–9.39) 0.002
2.54(1.54–4.22) < 0.001 1.20 0.32 3.34(1.80–6.18) < 0.001
children from families with low education level were be-
hind in preschool skills [5]. This may be due to various
factors related to low education level and socioeconomic
status, including the family’s inability to provide children
with supplies to support their development, establish ef-
fective communication, meet children’s social and physi-
cal needs, and provide an appropriate environment for
children to utilize their skills. Malnutrition due to poverty
may be another factor further compounding the problem.
In our study, birth order was associated with DD, but the
relationship was not significant in the multivariable model.
Ozkan et al. determined that family socioeconomic factors
had a greater impact on development under the age of 5 years
than biological factors, and that family socioeconomic status
and maternal/paternal education level were major risk factors
for DD. Furthermore, the authors noted that among children
whose Denver scale results indicated suspected DD, those
from families with three or more children had significantly
higher test scores when compared with those from families
with one or two children [15].
In our study, we found that a consanguineous marriage
increased the risk of DD by 3.99-fold (95%CI 1.69–9.40).
Similarly, Torabi et al. reported a 1.84-fold increase in DD
[23] and Kumar et al. reported a 5.09-fold increase in DD
[11] in families with consanguineous marriage.
As the control group in our study was age- and sex-
matched, we did not investigate the effect of sex on DD.
The strengths of our study include the population-
based samples from a cross-sectional linked study. We
also recognize some limitations. We assessed DD with a
parent-completed screening tool, the ASQ-TR.
Developmental screening tools are considered to be reli-
able measures for identifying DD in pediatric populations
[21]. However, as with all cross-sectional studies, the an-
swers provided by mothers on the questionnaire may be
incomplete or inaccurate due to recall bias. This may have
influenced our results.

In conclusion, DD can be identified early during well-child
visits. In such cases, it is critical for the health of the child and
community to screen for possible risk factors, eliminate the
causes when possible, and refer families to rehabilitation ser-
vices when necessary. Further studies identifying risk factors
are needed to improve these services, and practitioners must
be made more aware of this important issue. These steps will
help improve the health of future generations.
Acknowledgements We thank the executive support of the Ministry of
Health, the Dokuz Eylul University School of Medicine, and Maya
Academia. The ASQ-TR was provided by Maya Academia. We also
acknowledge the sincere cooperation of Dr. Dilek Guldal, Dr. Nilgun
Ozcakar, and Dr. Ferhat Demirci and all the family physicians who helped
in this study.
Authors’ Contributions Aylin Demirci, Mehtap Kartal conceived the pro-
ject, prepared the questionnaires, analyzed the data, and wrote the paper.
Aylin Demirci applied the ASQ-TR and the prepared questionnaires to
mothers on a voluntary basis via face-to-face interview.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Informed consent The Non-Interventional Research Ethics Committee
of Dokuz Eylul University School of Medicine (resolution number
2012/41–01 dated 17.12.2012) approved the study. Necessary permis-
sions were also obtained from the Ministry of Health, Turkish Public
Health Institution, and the Governorship of Izmir, Director of Public
Health, to conduct the study in primary healthcare centers (PHC). The
families and/or primary care physicians of children who were found to be
at risk for DD at the end of the evaluation were given additional informa-
tion about monitoring and further examination. All procedures performed
were in accordance with the ethical standards of the institutional and/or
national research committee and with the 1964 Helsinki declaration and
its later amendments or comparable ethical standards. Due to the nature of
the research present, however, no informed consent was required from the
individual participating in the study.
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