The Turkish Journal of Pediatrics
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Family and Infant Characteristics in Relation to Age at Walking in Turkey
S. Songül Yalçın1, Kadriye Yurdakök1, Başak Tezel2, Sema Özbaş2
1Social Pediatrics Unit, Departments of Pediatrics, Hacettepe University Faculty of Medicine, and 2Ministry of Health,
Directorate of Mother and Child Health and Family Planning, Ankara, Turkey
|The purpose of this study was to assess the onset of independent ambulation
relative to possible relationships with maternal and infant characteristics. In
a cross-sectional study, the health files of 1,553 Turkish children aged 12-23
months were selected by the multistage sampling method in the Nomenclature
of Territorial Units for Statistics (NUTS) regions coded as low, medium and
high malnutrition levels in Turkey. Children were selected from health centers
by systematic sampling technique in each region. Kaplan-Meier analysis and
estimated mean values were used for data description; log-rank test and
the Cox multivariable regression analysis were applied for data analysis.
Maternal education level, occupation, region of residence, gestational iron
supplementation, child’s gender, child’s nutritional status, and presence
of anemia in the infant during the survey period demonstrated significant
relationships with walking unassisted in the univariate analysis. However,
multivariable analysis showed that high maternal education, absence of
parental consanguinity and appropriate weight-for-age Z score were positively
associated with earlier age of walking. These findings showed the importance
of improvement in girls’ education, prevention of postnatal growth retardation
and improvement in diet quality for children’s gross motor development.
In addition, counseling programs should be given to decrease the rate of
walking age, consanguinity, growth, girls’ education.
|Several studies have shown wide variations
in the achievement of independent walking
in healthy infants-. Walking attainment is
a complex developmental process driven by
a wide variety of genetic and environmental
factors. Physical growth in length and weight,
nutrient and micronutrient intake, muscle
and bone tissue strength, maturation of the
nervous system, cognitive development, quality
of the home environment, stimulation and
positive care-giving, and cultural and childrearing
practices play a role in the initiation
of walking without support,-. Healthy infants
begin to walk around 12 months with some
biological variability. By the age of 18 months,
all healthy term infants attain walking ability.
Later achievement of walking is an indicator
of developmental disorders (cerebral palsy,
psychomotor retardation)-. Therefore, the
age of independent walking attainment may
provide valuable clues about the overall health
and development of infants. Studies are limited
on the predictors for walking attainment.
The purpose of this study was to determine
the effect of some demographic, social and
infant characteristics (gender, birth order,
maternal education, working status, family
characteristics, infantile growth parameters,
presence of anemia) on the age at walking
without support among healthy children
aged 12-23 months, already involved in a
cross-sectional study to observe the effect of
nationwide iron supplementation.
|Material and Methods |
|The data were collected in the course of a
cross-sectional study on the prevalence of
anemia that was carried out in 2007 in three
NUTS-1 (Nomenclature of Territorial Units for Statistics) regions of a total of 12 NUTS
regions of Turkey. The study population
consisted of 12-23-month-old children, living
in three different NUTS-1 regions of Turkey
according to the prevalence of malnutrition (the
percentages of height-for-age below -3SD; high,
middle and low) in the Turkey Demographic and
Health Survey (TDHS) 2003 and with “region
with high malnutrition prevalence” defined as
poor region, “region with middle malnutrition
prevalence” as middle region and “region with
low malnutrition prevalence” as good region.
The detailed protocol was given before,.
Any children who were extreme premature
(<32 weeks), who had a condition preventing
them from walking, birth weight less than 1500
g, an abnormal birth history, or a history of
intensive care unit admissions, developmental
problems, developmental hip dysplasia, or
neuromuscular diseases were eliminated from
the original data as were those who had a vague
or unclear history. This study was reviewed
and approved by the Ethical Committee of the
Turkish Ministry of Health. Written informed
consent was obtained from caretakers for each
participant before enrollment.
Trained field workers made home visits and
completed a questionnaire. The questionnaire
provided information concerning the reason
for the visit, gender, birth order, and child’s
health and age at independent ambulation.
Anthropometric measurements of children
were obtained by trained field workers.
Standardization sessions were conducted during
training and the course of data collection.
Z scores of weight-for-age, weight-for-height,
height-for-age, and body mass index for age
(WAZ, WHZ, HAZ, and BAZ, respectively)
were calculated from the World Health
Organization (WHO) Multicentre Growth
Reference Study (MGRS). Due to the limited
number of cases below -2 WAZ (n=15), WHZ
(n=21) and BAZ (n=25), comparisons were
done for cases below -1 and above 1 Z scores.
Age at walking was defined as the age at which
the subject was able to arise from a sitting
position on the floor and walk at least 6 feet
without support. Birth order was classified
into one of three groups as first-, second- or
Capillary blood samples were obtained in two
microtubes from the middle finger of the left
hand of each subject using a microlance, and
centrifuged to measure the hematocrit (Htc)
levels. If the mean Htc value of a child was less
than 33%, venous blood samples were taken
for complete blood count [Hemoglobin (Hb),
Htc and mean corpuscular volume (MCV) by
STKS Coulter Machine]. Anemia was defined
as Hb <11.0 g/dl, MCV <70 fL and red cell
distribution width >14.5%,.
All analyses were performed with the Statistical
Package for the Social Sciences (SPSS) for
Windows (SPSS Inc., Chicago, IL, USA). The
age at walking unassisted was calculated by
the Kaplan–Meier method, and the differences
were analyzed by a log-rank test. P values
<0.05 were considered significant. Estimated
means and standard errors were calculated.
Cox regression models [Method = Backward
Stepwise (Likelihood Ratio); probability
for stepwise was 0.05 for entry and 0.10
for removal] were performed to assess the
impact of factors including region of residence,
maternal age (<25, 25-29, 30-34, ≥35),
maternal education level (≥8 vs <8 years),
maternal occupation (working vs housewife),
parental occupation, family type (nuclear vs
extended), parental consanguinity (absence
vs presence), breastfeeding duration (≥6
vs <6 mo), infant gender, sibling under 5
years of age (presence vs absence), low birth
weight or premature (absence or presence),
birth order (first vs second and upper),
iron supplementation of infant (present vs
absent), vitamin supplementation of infant
(multivitamin, vitamin D vs nothing),
gestational iron supplementation (no, third,
second trimester vs first trimester), infant
anemia during the study period (present vs
absence), WAZ (-1-0.99 Z score or ≥1 Z score
vs <-1 Z score), HAZ (1-0.99 Z score or ≥1
Z score vs <-1 Z score). Hazard ratios with
95% confidence intervals (CI) were used to
quantify the strength of these associations.
|The study sample consisted of 1553 children
(816 males, 737 females). Overall, 26.1% of
children were from a low malnutrition region,
34.3% from a moderate region and 39.6%
from a high malnutrition region. Mean (±SD) maternal age was 28.1 (±5.6) years. Maternal
educational status was low; only 33.6% had
completed primary school (≥8 years). Only
7.4% of mothers were working. Approximately
23.1% were from an extended family.
The mean age (±SD) of infants was 18.0
(±3.6) months. The mean (±SD) birth weight
of the enrolled children was 3.22 (±0.60) kg;
about 8.8% of children were born premature
and 7.4% had birth weight <2.5 kg. Overall,
14.5% of children in the study group were
born premature or had low birth weight.
37.3% of children in the sample were the firstborn.
Breastfeeding was widespread; 98.6% of
children were ever breastfed and 18.9% received
breast-milk less than 6 months. Mean (95%
CI; lower, upper bound) WAZ, HAZ, WHZ,
and BAZ scores at birth were 0.51 (0.46,
0.56), -0.19 (-0.27, -0.11), 0.81 (0.75, 0.87),
and 0.89 (0.82, 0.95), respectively. Overall,
7.9% of children had anemia. Mean (±SD)
Htc level was 35.4 (±2.5)%. During study
period, the estimated mean walking age of all
study participants was 12.42 months, with a
standard error of 0.06 month.
Univariate analyses showed that the mean age
at walking without support was the youngest
in the low malnutrition region and the oldest
in high malnutrition region (Table I). Maternal
age did not affect the walking age of children.
Parental educational level (<5 years, 5-7
years, 8-10 years, 11-14 years and ≥15 years) showed a “U”-shaped interaction with the
age of walking; maternal education level
between 8-14 years and paternal education level
between 11-14 years had the earliest age for
walking unassisted. There were no significant
differences according to paternal occupation,
family type, presence of social security of the
family, number of household members, or
presence of any sibling under 5 years of age.
| ||Table I. The Age of Walking without Support in Turkish Children 12-23 Months of Age According to
Some Family Characteristics (Log Rank [Mantel-Cox])|
Table II lists the descriptive statistics for age
at independent ambulation across gestational
characteristics: presence of iron deficiency
anemia (IDA), iron supplementation, birth type,
birth interval and birth order, gestational age,
and birth weight. Neither birth interval nor
birth order was significantly associated with
walking age in the univariate analyses. There
were no differences according to maternal
history of anemia. Interestingly, the mean
age for walking without support was younger
in children with mothers who received iron
supplementation during the first trimester of
gestation compared to the others.
The effect of some infant characteristics on
age at walking unassisted is given in Table
III. Among factors examined, females walked
earlier than males. History of iron and vitamin
supplementation during the first year of life
was not associated with age of walking without
support. However, children with anemia and
palmar pallor had an older age of walking
without support than non-anemic ones. In
cases with infants whose breastfeeding duration
was less than 6 months of age, the mean
age at walking attainment was older than in
the others. Birth weight was not significantly
associated with walking attainment (Table II),
but growth parameters during the study period
were associated with attainment of walking;
children with WAZ <-1 or HAZ <-1 had
walked at a later age than the others.
Cox backward-stepwise regression analysis
confirmed that the age at walking was younger
in children with high maternal education level
(≥8 years), longer breastfeeding duration (≥6
mo), absence of parental consanguinity, and
appropriate WAZ (≥-1 Z score) compared to
others (Table IV).
|The mean age at walking attainment was
12.42 months (95% CI 12.30-12.54) in the
present study. The ages at which children
start to walk vary considerably. Based on data
from five countries, the WHO MGRS Group
developed normal age ranges for achievement of
motor milestones among healthy children and
reported that the mean age (SD) for walking
alone was 12.1 (1.8) months (1st and 99th
percentiles in months 8.2 and 17.6). Several
factors, namely differences in the definition of
motor milestones, the methods and frequency
of data collection, child-rearing practices, and
genetics could explain the variations around the
world in the age of walking without support.
Differences in residence in the present study
might be partly explained by differences in
child-rearing practices and genetics. In addition,
in the present study, walking attainment was
inversely associated with HAZ and WAZ.
Differences in nutritional status could have
an additional role in development. The MGRS
found that relationships among anthropometric
indicators and accelerations in ages of milestone
achievement or delays, even if small, appeared
to vary qualitatively in healthy populations
with respect to specific motor milestones.
The associations between motor development
and states of undernutrition were reported
previously ,,,. Physical growth may constrain
gross motor development. Children in some
developing countries begin to walk 1.5–3 months
later than their well-nourished American or
European counterparts,. In a cross-sectional
study of infants, stunting was associated with
slower acquisition of locomotive milestones
(i.e., crawling, walking) compared with
developmental norms from a healthy United
States (US) sample. Similarly, length was
positively related to motor development scores
in 12- and 18-month–old Indonesian children,
and stunting was associated with a delay in
walking unassisted in Zanzibari and Nepali
children,,. In Guatemala, growth in length
and weight during the first year of life predicted
the age at walking unassisted. Furthermore,
in Pakistani infants, changes in LAZ from 0 to
6 months were inversely associated with age
at commencement of independent walking.
In addition, supplementation was known to
improve motor development in nutritionally at
risk infants/toddlers,. A possible explanation
is that growth retardation and poor diet
may directly affect the developing central
nervous system, resulting in disturbances in brain maturation, particularly affecting
the division of cortical cells, coordinated
development of the dendritic synaptic apparatus
of neurons, myelinization, and the activity of
| ||Table II. The Age of Walking without Support in Turkish Children 12-23 Months of Age According to
Some Gestational Characteristics (Log Rank [Mantel-Cox])|
This study indicated that there was no
significant association between some birth
characteristics (birth weight, gestational age,
interval, twin pregnancies) and walking age.
Firstborns did not reach independent walking
any earlier than their subsequent siblings.
However, the ability of this study to prove
this with certainty is somewhat limited by the
design of the sampling method. Mostly, low
birth weight and premature infants might have
postpartum problems; however, children with
disabilities, mechanical ventilation and sepsis
were not included into the study. In addition,
the present study did not include very low
birth weight and premature infants. Similar
to the present study, Kuklina et al. found
that growth in length and weight during the
first year of life, rather than size at birth, had
predicted age of walking.
| ||Table III. The Age of Walking without Support in Turkish Children 12-23 Months of Age According to
Some Infant Characteristics (Log Rank [Mantel-Cox])|
Several micronutrients such as iron, zinc and
essential fatty acids have been proposed to
play a role in child development,,,,. As
seen in the present study, iron deficiency (ID)
and IDA have been associated with lower
scores on global tests of motor development.
Zanzibari children who were neither anemic
nor ID were 66% more likely to be walking
unassisted than those who were anemic with
or without ID. In addition, Nepali children who were anemic were less likely to be walking
than those who were not anemic. Olney et
al. reported that children who received any
iron walked unassisted sooner than those who
received no iron, and this effect was stronger in
those who had IDA at baseline. On the other
hand, Perez et al. focused on the effects of
ID in mothers with regard to the potential
negative effect of poor maternal functioning
on infant development and mother-infant
interactions. Indeed, the present study showed
that maternal iron supplementation during the
early gestational period was associated with
earlier walking unassisted.
| ||Table IV. The Factors That Affect the Age of Walking Unassisted in Turkish Children 12-23 Months of Age,
Multivariate Analysis Cox Regression (Backward Stepwise)|
Breastfeeding could affect infant development.
Certain constituents of breast-milk (e.g.,
docosahexaenoic acid) are known to be
associated with infant mental development,
but there is little evidence that they affect motor
development. On the other hand, Vestergaard
et al. reported that achievement of two motor skills (crawling and pincer grip) was linked to
the duration of breastfeeding in a large sample
of Danish infants, even after adjustment for
potentially confounding variables. The present
study showed that ever breastfed infants and
infants breastfed more than 6 months walked
earlier. However, no significant change was
detected in cases breastfed more than 11
months (the estimated mean months for
walking attainment were 12.39 for children
breastfed more than 11 months and 12.28 for
children with breastfeeding duration between
6-11 months). Some possible mechanisms
include differences in maternal caregiving or
infant motivation to explore the environment or
be upright,,, all of which could be altered
by the amount of time spent nursing. In the
present study, unassisted walking also depended
on maternal education and occupation. It
is known that maternal education improved
infant development. Lung et al. showed
that the maternal education directly affected
gross motor development at 18 months and
all four dimensions of gross motor, fine motor,
language, and social development at 36 months
by a further analysis of structural equation
modeling. Forns et al. reported that maternal
educational attainment was strongly related to
child mental test scores at 14 months using
Bayley Scales of Infant Development. In turn,
Barros et al. reported that low maternal
education was found to be an important
predictor of neuropsychological developmental
problems in different contexts. Education
can serve as the factor required to help the
mother obtain the resources she needs to
improve her child-rearing behavior . Educated
women might offer better parenting, involving
factors such as lifestyle, healthcare, housing,
and the provision of a cognitively stimulating
Delays in motor milestone acquisition were
found in the presence of parental consanguinity
in the present study. This might be explained by
the poor quality of child-rearing environmental
factors including low maternal education. Also,
it is known that high consanguinity can be a
contributing factor to the high incidence of
some rare autosomal recessive neurometabolic
diseases. However, the rate of consanguinity
has been approximately 20-25% in Turkey.
Girls in the MGRS tended to achieve milestones
at earlier ages than did boys. However, the
magnitude of the observed differences is too
small to justify sex-specific norms. In the
present study, univariate analysis showed that
unassisted walking also depended on gender;
girls walked sooner than boys. However,
there were no differences in gender in the
The strengths of this multicenter study include
its design as a large cross-sectional study,
use of standardized protocols and analysis at
the same time of several factors that might
influence walking. There are some limitations
of the study. First, no data were collected to
validate the mothers’ reports of their infants’
motor skills. Additional data on measures such
as social support and directly measured parentchild
interaction (including abuse, neglect) and
child-rearing practices should be included in
future investigations. For example, children
who are carried a lot or not encouraged to
move around may start to walk later. Although
we analyzed maternal factors such as age,
education, occupation, and family size, as well
as infant birth order, these variables may not
serve as adequate proxies of factors such as
socioeconomic status, parent-child interaction and quality of the home environment.
Our results indicate the importance of:
prevention of postnatal growth retardation,
improvement in diet quality for the child and
iron supplementation during the gestational
period, maternal education (girls’ education),
and prevention of parental consanguinity with
pre-marriage counselling programs.
We are grateful to the infants and their mothers
for their willingness to participate in the
study. We are indebted to the health workers
and doctors of the primary health care center
whose dedication and effort made this project
possible and to the Advisory Board of the “Iron
like Turkey” program of the Turkish Ministry
of Health, without whose encouragement and
support this project could never have been
Sources of Funding
The cost of the participant health workers in
the fieldwork, laboratory work and data entry
was supported by the ADEKA, Abdi İbrahim,
1. Adolph KE, Vereijken B, Shrout PE. What changes in
infant walking and why. Child Dev 2003; 74: 475-497.
2. Kariger PK, Stoltzfus RJ, Olney D, et al. Iron deficiency
and physical growth predict attainment of walking but
not crawling in poorly nourished Zanzibari infants. J
Nutr 2005; 135: 814–819.
3. Kuklina EV, Ramakrishnan U, Stein AD, Barnhart HH,
Martorell R. Growth and diet quality are associated
with the attainment of walking in rural Guatemalan
infants. J Nutr 2004; 134: 3296–3300.
4. Birengen Z, Emde RN, Campos JJ, Appelbaum MI.
Affective reorganization in the infant, the mother and
the dyad: the role of upright locomotion and timing.
Child Dev 1995; 66: 499-514.
5. Groos AD. Delayed motor development in relation to
nutritional status among children under two years of
age in two districts of Simbu Province. P N G Med J
1991; 34: 238-245.
6. Jahari AB, Saco-Pollitt C, Husaini MA, Pollitt E. Effects
of an energy and micronutrient supplement on motor
development and motor activity in undernourished
children in Indonesia. Eur J Clin Nutr 2000; 54 (Suppl):
7. Pollitt E. Developmental sequel from early nutritional
deficiencies: conclusive and probability judgements. J
Nutr 2000; 130: 350S-353S.
8. Allen MC, Alexander GR. Screening for cerebral palsy
in preterm infants: delay criteria for motor milestone
attainment. J Perinatol 1994; 14: 190–193.
9. Johnson A, Goddard O, Ashurst H. Is late walking
a marker of morbidity? Arch Dis Child 1990; 65:
10. Silva PA, McGee R, Williams S. The predictive
significance of slow walking and slow talking: a report
from the Dunedin Multidisciplinary Child Development
Study. Br J Disord Commun 1982; 17: 133–139.
11. Yalcin SS, Pekcan G, Tezel B, et al. 12-23 aylık
çocuklarda demir kullanım araştırması raporu. Ankara.
Ana Çocuk Sağlığı Aile Planlaması Genel Müdürlüğü
Matbaası. 2009. [in Turkish]
12. Hacettepe University Institute of Population Studies.
Turkey Demographic and Health Survey, 2003.
Hacettepe University Institute of Population Studies,
Ministry of Health General Directorate of Mother and
Child Health and Family Planning, State Planning
Organization and European Union. Ankara. 2004.
13. World Health Organization. Child Growth Standards.
http://who.int/childgrowth/software/en/ [last accessed
14. United Nations Children’s Fund, United Nations
University, World Health Organization. Iron Deficiency
Anaemia Assessment, Prevention and Control. A guide
for programme managers. WHO/NHD/01.3. World
Health Organization. 2001. http://www.who.int/
control.pdf [last accessed January 2011].
15. WHO Multicentre Growth Reference Study Group. WHO
Motor Development Study: windows of achievement
for six gross motor development milestones. Acta
Paediatr Suppl 2006; 450: 86-95.
16. Goetghebuer T, Ota MO, Kebbeh B, et al. Delay in
motor development of twins in Africa: a prospective
cohort study. Twin Res 2003; 6: 279-284.
17. WHO Multicentre Growth Reference Study Group.
Relationship between physical growth and motor
development in the WHO Child Growth Standards.
Acta Paediatr Suppl 2006; 450: 96-101.
18. Cheung YB, Yip PS, Karlberg JP. Fetal growth, early
postnatal growth and motor development in Pakistani
infants. Int J Epidemiol 2001; 30: 66-72.
19. Pollitt E, Husaini MA, Harahap H, Halati S, Nugraheni
A, Sherlock AO. Stunting and delayed motor
development in rural West Java. Am J Hum Biol
1994; 6: 627–636.
20. Siegel EH, Stoltzfus RJ, Kariger PK, et al. Growth
indices, anemia, and diet independently predict motor
milestone acquisition of infants in south central Nepal.
J Nutr 2005; 135: 2840–2844.
21. Walka H, Pollitt E. A preliminary test of a developmental
model for the study of undernourished children in
Indonesia. Eur J Clin Nutr 2000; 54 (Suppl ): S21–37.
22. Olney DK, Pollitt E, Kariger PK, et al. Combined iron
and folic acid supplementation with or without zinc
reduces time to walking unassisted among Zanzibari
infants 5- to 11-mo old. J Nutr 2006; 136: 2427-2434.
23. Wainwright PE. Dietary essential fatty acids and brain
function: a developmental perspective on mechanisms.
Proc Nutr Soc 2002; 61: 61–69.
24. Yalçın SS. Effects of iron deficiency on development
and behaviour. In: Coşkun T (ed). Iron: Absorption,
Metabolism and Deficiency. Ankara: Danone Institute
Turkey Association, Pelin Ofset; 2010: 37-45.
25. Perez EM, Hendricks MK, Beard JL, et al. Motherinfant
interactions and infant development are altered
by maternal iron deficiency anemia. J Nutr 2005; 135:
26. Schack-Nielsen L, Michaelsen KF. Advances in our
understanding of the biology of human milk and its
effects on the offspring. J Nutr 2007; 137 (Suppl):
27. Vestergaard M, Obel C, Henriksen TB, Sørensen HT,
Skajaa E, Ostergaard J. Duration of breastfeeding and
developmental milestones during the latter half of
infancy. Acta Paediatr 1999; 88: 1327-1332.
28. Walker SP, Wachs TD, Grantham-McGregor S, et al.
Inequality in early childhood: risk and protective factors
for early child development. Lancet 2011; 378: 1325-
29. Lung FW, Shu BC, Chiang TL, Lin SJ. Maternal mental
health and childrearing context in the development
of children at 6, 18 and 36 months: a Taiwan birth
cohort pilot study. Child Care Health Dev 2011; 37:
30. Forns J, Julvez J, García-Esteban R, et al. Maternal
intelligence-mental health and child neuropsychological
development at age 14 months. Gac Sanit 2012 Jan
26. [Epub ahead of print].
31. Barros AJ, Matijasevich A, Santos IS, et al. Child
development in a birth cohort: effect of child
stimulation is stronger in less educated mothers. Int
J Epidemiol 2010; 39: 285–294.
32. Tunçbilek E, Ozgüç M. Application of medical genetics
in Turkey. Turk J Pediatr 2007; 49: 353-359.
33. WHO Multicentre Growth Reference Study Group.
Assessment of sex differences and heterogeneity in
motor milestone attainment among populations in
the WHO Multicentre Growth Reference Study. Acta
Paediatr Suppl 2006; 450: 66-75.
[Mail to Editor ]