 CHILDREN’S ORTHOPAEDICS
Is prematurity a risk factor for developmental
M. M. Orak,
T. Onay,
S. A. Gümüştaş,
T. Gürsoy,
H. H. Muratlí
From Zeynep Kamil
Education and
Research Hospital,
Istanbul, Turkey
 M. M. Orak, MD, Orthopaedic
Surgeon, Department of
Orthopaedics and
Traumatology
Fatih Sultan Mehmet Training
and Research Hospital,
Istanbul, Turkey
 T. Onay, MD, Orthopaedic
Surgeon, Department of
Orthopaedics and
Traumatology
Marmara University Pendik
Training and Research Hospital,
Istanbul, Turkey
 S. A. Gümüştaş, MD,
Orthopaedic Surgeon
Yavuz Selim Bone disease and
Rehabilitation Hospital,
Department of Orthopaedics
and Traumatology, Trabzon,
Turkey
 T. Gürsoy, MD, Paediatrician,
Associate Professor, Neonatal
Intensive Care Unit
Zeynep Kamil Maternity and
Children's Training and
Research Hospital, Istanbul,
Turkey
 H. H. Muratlí, MD,
Orthopaedic Surgeon,
Professor, Department of
Orthopaedics and
Traumatology
Fatih Sultan Mehmet Training
and Research Hospital
Department, Istanbul, Turkey
Correspondence should be sent
to Dr Med M. M. O. Orak;
e-mail:
mehmetmufitorak@yahoo.com
©2015 The British Editorial
Society of Bone & Joint
Surgery
doi:10.1302/0301-620X.97B5.
34010 $2.00
Bone Joint J
2015;97-B:716–20.
Received 22 February 2014;
Accepted after revision 5
January 2015
716
dysplasia of the hip?
A PROSPECTIVE STUDY
The aim of this prospective study was to investigate prematurity as a risk factor for
developmental dysplasia of the hip (DDH). The hips of 221 infants (88 female, 133 male,
mean age 31.11 weeks; standard deviation (SD) 2.51) who were born in the 34th week of
gestation or earlier, and those of 246 infants (118 female, 128 male, mean age 40.22 weeks;
SD 0.36) who were born in the 40th week of gestation, none of whom had risk factors for
DDH, were compared using physical examination and ultrasound according to the technique
of Graf, within one week, after the correction of gestational age to the 40th week after birth
or one week since birth, respectively. Both hips of all infants were included in the study.
Ortolani’s and Barlow’s tests and restricted abduction were accepted as positive findings on
examination. There was a statistically significant difference between pre- and full-term
infants, according to the incidence of mature and immature hips (p < 0.001). The difference
in the proportion of infants with an α angle < 60° between the two groups was statistically
significant (p < 0.001). The incidence of pathological dysplasia (α angle < 50 º) was not
significantly different in the two groups (p = 1.000). The Barlow sign was present in two
(0.5%) pre-term infants and in 14 (2.8%) full-term infants.
These results suggests that prematurity is not a predisposing factor for DDH.
Cite this article: Bone Joint J 2015; 97-B:716–20
Developmental dysplasia of the hip (DDH) can Patients and Methods
be diagnosed by both physical examination This prospective study had ethical approval,
and radiological investigation. Barlow’s1 and and parents of the infants participating in the
Ortolani’s2 signs and limited abduction are the study gave informed consent.
most valuable physical findings.3 All infants who were included in the study
For infants aged < six months, the ultra- were born in our hospital between August 2012
sonographic investigation of the hip developed by and August 2013. After evaluation by a neona-
Graf4 in the 1980s has been widely used for the tal paediatrician (TG), all those with no risk fac-
radiological evaluation of DDH.5 He proposed a tors for DDH, such as a family history of DDH
classification that was based on the angles formed or breech presentation, the presence of torticol-
by the sonographic structures of the hip: class I lis, deformity in the spine or lower limbs, were
hips are normal, class II hips are either immature referred to an orthopaedic surgeon (MMO) for
or somewhat abnormal, class III hips are sub- evaluation of their hip. A total of 467 infants
luxed and class IV hips are dislocated. were included in the study, and the risk factor
Graf6 emphasised the importance of gestational chosen for investigation was prematurity.
age for the ultrasonographic classification of Inclusion criteria were as follows: gesta-
dysplasia of the hip in pre-term infants. He clas- tional age ≤ 34 weeks for pre-term infants and
sified DDH according to chronological age, but 40 weeks for full-term infants. Babies born
assigned the diagnosis of pathological dysplasia with a gestational age of 35 to 39 weeks were
and formulated treatment by considering the excluded. Exclusion criteria also included
corrected age. those with genetic disorders, neuromuscular
Only a few studies have dealt with the influ- disease, neural tube defects, congenital foot
ence of gestational age on the development of anomalies and oligohydramnios.
DDH.7-10 The aim of this study was to investi- A total of 10 182 infants were born during
gate prematurity as a risk factor for DDH by the study period (Table I), 495 of whom had a
comparing the sonographic development of gestational age ≤ 34 weeks. Of these, 221 (88
the hips of pre-term and full-term infants. girls; 39.8% and 133 boys; 60.2%) with a
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 IS PREMATURITY A RISK FACTOR FOR DEVELOPMENTAL DYSPLASIA OF THE HIP? 717

Table I. The distribution of gestational age of the infants

Birth week n Evaluated Included %

≤ 34 495 274 221 44
35 to 39 6023 Not included Not included
40 2402 278 246 10
41 to 42 1262 Not included Not included
Total 10 182 467

10182 live born infants

495 infants had a gestational 2402 infants had a gestational age

age ≤ 34 wks of 40 wks

15 had positive family history

68 had breech presentation
39 had oligohidramnios 278 infants were evaluated on Monday
23 had congenital anomaly
61 died 5 had positive family history
9 parents did not sign the 8 had breech presentation
informed consent form 7 had oligohidramnios
59 infants were lost to follow-up 2 had congenital anomaly
10 parents did not sign the
informed consent form
221 pre-term infants were included

246 term infants were included

Fig. 1

Flowchart showing the inclusion of infants at pre-term and term.

mean gestational age of 31.11 weeks (24 to 34; SD 2.51)
were included in the study (Fig. 1).
A total of 2402 were born at full term. Of these, 278
were evaluated by the senior author (MMO) and 246 (118
girls; 48% and 128 boys; 52%) were included in the study
(Fig. 1).Their mean gestational age was 40.2 weeks (39.7 to
40.9; SD 0.36).
Whereas the full-term infants underwent ultrasound
within the first postnatal week, the 221 premature infants
had their assessments at the gestational age of 40 weeks,
regardless of their actual birth week.
All the infants were examined clinically regardless of ges-
tational age using Barlow’s1 and Ortolani’s2 manoeuvre,
and the findings were recorded. In addition, any limitation
of abduction of the hips was recorded. Ultrasound exami-
nation was performed on the same day to evaluate the hip.
The same orthopaedic surgeon (MMO), who had > ten
years’ experience in paediatric practice, undertook all the
physical and ultrasound examinations. The ultrasound
evaluation was carried out on a special hip ultrasound
table, which supports the infant in the lateral decubitus
position in accordance with the Graf technique.4 Both hips
were examined. All ultrasound scans were performed using
a 7.5 MHz linear transducer (SDU-2200, Pro-Shimadzu,
Kyoto, Japan). The images were assessed in standard fash-
ion on a sonogram which had a straight iliac wing contour,
acetabular labrum and a visible lower limb of the ilium in
the acetabular fossa), measured and classified according to
Graf.4 Based on the ultrasound measurement of the α angle
which indicates the bony roof and mainly determines the
type of hip, those infants whose α angle was ≥ 60° formed
group 1 (mature), those with an angle between 50° and 59°
formed group 2 (immature), and those with an angle of ≤
49° formed group 3 (pathological). The β angle, which indi-
cates the cartilage acetabular roof and is used to determine
the subgroups, was also measured.
Statistical analysis. The Number Cruncher Statistical
System (NCSS, 2007) and the statistical software Power
Analysis and Sample Size (PASS, 2008) (NCSS, Kaysville,
Utah) were used. Data from both hips in all babies were
included. In addition to descriptive statistical methods
(mean, standard deviation (SD), frequency), the Fisher–
Freeman–Halton exact test with Bonferroni adjustment
was used to evaluate hip maturity. The Student’s t-test was
used to compare the mean difference of the β angles
between two groups. Pearson’s correlation coefficient was

VOL. 97-B, No. 5, MAY 2015

718 M. M. ORAK,T. ONAY, S. A. GÜMÜŞTAŞ, T. GÜRSOY, H. H. MURATLÍ

Table II. The α angle measurements and gender distribution in pre-term and full-term infants

Pre-term infants (n = 221) Full-term infants (n = 246)

(n = 467) n (%) n (%) p-value*

α angle < 60° 6 (2.7) 70 (28.5) < 0.001

≥ 60° 215 (97.3) 176 (71.5)
Gender Female 88 (39.8) 118 (48.0) 0.047
Male 133 (60.2) 128 (52.0)
* Fisher’s exact test

Table III. Evaluation of maturity of the hip in pre- and full-term infants

Pre-term infants (n = 221) Full-term infants (n = 246)

(n = 467) n (%) n (%) p-value
Both hips mature 215 (97.3) 176 (71.5) < 0.001
One hip mature/other immature 5 (2.3) 48 (19.5)
Both hips immature 0 (0.0) 21 (8.5)
One hip mature/other pathological 1 (0.5) 0 (0.0)
Both hips pathological 0 (0.0) 1 (0.4)

Table IV. Correlation between α and β angles and gestational age in pre-term
infants according to gender

Female (n = 88) Male (n = 133)

(n = 221) R-value p-value R-value p-value
Right α -0.132 0.222 -0.300 0.001
Right β 0.232 0.029 -0.024 0.780
Left α -0.155 0.148 -0.210 0.016
Left β 0.106 0.326 0.058 0.505

used to analyse associations between α and β angles and
gestational age. The effects of hip side, gender and gesta-
tional age group (i.e. pre-term or full-term) on the α angle
were analysed with a generalised linear mixed-effects
model, and statistical significance was set at p < 0.05.
Results
The difference in the total number of male infants between
the pre-term and full-term groups was statistically signifi-
cant (Fisher’s exact test, p = 0.047). (Table II)
For all infants, the correlation between the α and β angles
of right and left hips was statistically significant (r = 0.669;
p < 0.001 and r = 0.524; p < 0.001, respectively).
The mean α angle was 69.78° (SD 4.84) in the pre-term
group and 62.95° (SD 4.74) in the full-term infants. There
was a statistically significant difference in the number of
infants with an α angle < 60° between pre-term and full-
term groups (p < 0.001, Fisher’s exact test,) (Table II). The
mean β angle was 56.67° (SD 7.85) in the pre-term infants
and 62.64° (SD 6.27) in full-term infants; the difference was
statistically significant (p < 0.001, Student’s t-test).
A statistically significant difference was found
between pre- and full-term infants according to the inci-
dence of maturity of the hip (p < 0.001, Fisher’s Exact
Test; Table III).
No difference was observed between pre- and full-term
groups for the number of pathological cases (p = 1.000
Fisher’s exact test).
Physical examinations found limited abduction in one
pre-term infant (0.2%) and in four full-term infants
(0.8%). Barlow’s sign was present in two pre-term infants
(0.5%) and 14 full-term infants (2.8%). Ortolani’s sign was
not found in any infant.
When the relationship between gestational age and ultra-
sound-determined maturity of the hip in the pre-term
infants was examined, a negative correlation was found
between gestational age and the α values of both right and
left hips in boys. There was a positive correlation between
gestational age and β values of the right hips in girls
(Table IV). However, the change in β angles was not influ-
enced by gestational age.
Generalised linear mixed-effects modelling was used to
analyse the fixed and random effects of the predictors on α
angles, which were dichotomised as either < 60° or ≥ 60°.
The main effects of gestational age and gender, and the
interaction between gestational age and gender, were con-
sidered to be fixed effects. Gestational age was regarded as
either pre- or full term. The hip side (right or left) nested
within subjects was added to the model as a random effect.
As a result, the main effect of gestational age on the α angle

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 IS PREMATURITY A RISK FACTOR FOR DEVELOPMENTAL DYSPLASIA OF THE HIP?
Table V. Mixed effects analysis of risk factors on the α angle
Source
Fixed effects Intercept
Group
Gender
Group/gender
Random effects Intercept
Subject (hip side)
OR, odds ratio, CI, confidence interval
was found to be statistically significant (odds ratio (OR)
0.043; 95% confidence interval (CI) 0.011 to 0.164;
p < 0.001). The main effects of gender, and the interaction
between gestational age and gender, were not statistically
significant. A likelihood-ratio test confirmed that adding
the random effects of intercept and hip side to the model,
offered significant improvement over a logistic regression
model with fixed effects only (p < 0.001) (Table V). A post
hoc power analysis of the OR of gestational age was found
to be 0.99, with a minimum of 32 infants in both groups,
being sufficient to show the statistical significance of the
effect of group on the α angle with a statistical power of
0.80.
Discussion
Breech presentation and family history are well-known risk
factors for DDH. Congenital dislocation of the knee, torti-
collis and deformities of the foot are anomalies which may
accompany DDH.11 These were thus exclusion criteria for
the infants in this study.
Infants who are born between the 35th and 37th gesta-
tional weeks are defined as late premature.12,13 Such babies
have fewer medical problems compared with premature
infants,14 and so infants born before 34 weeks’ gestational
age were included in this study.
Most unstable hips detected at birth will stabilise
quickly. Weinstein15 cited several studies showing that 22%
will become normal in infants in whom diagnosis is made
before three months of age and 88% in those in whom the
diagnosis is made before two months of age. There are few
reports comparing the findings on physical examination for
DDH between pre- and full-term infants. In their study,
where screening for DDH was performed by physical
examination, Yiv et al16 found fewer unstable hips in pre-
mature infants than in full-term infants. Similarly, we found
fewer positive Barlow signs in pre-term infants. The mean
chronological age of our pre-term group was 8.9 weeks (6
to 16) at the time of examination, whereas the full-term
group was evaluated within one week of birth. The differ-
ence in the findings on physical examination might be due
to the pre-term infants being chronologically older.
The influence of gestational age on DDH is debatable, as
DDH is not well defined in premature infants.17 Although
there are studies which suggest that premature birth is a
VOL. 97-B, No. 5, MAY 2015
719
95% CI
z-value p-value OR Lower Upper
1.83 0.067 4.115 0.905 18.719
–4.59 < 0.001 0.043 0.011 0.164
0.68 0.497 2.579 0.168 39.695
–1.16 0.245 0.232 0.020 2.725
- - 2.813 0.601 13.169
- - 0.005 9.42e-24 1.06e+17
risk factor for DDH,18,19 others suggest that it is actually
protective against it.10,20 We found no difference between
the incidence of pathological hips requiring treatment, but
the incidence of immature hips in infants born prematurely
was found to be significantly lower.
Some studies have suggested that DDH of the hip is
observed less often in premature infants. Sezer et al21
considered gestational age and birth weight to be risk in
premature infants, but could not show any influence of
these factors on DDH. Similarly, Dogruel et al22 suggested
that prematurity was not a risk factor for DDH.
A study by Langer and Kaufmann8 found significantly
more Graf type 2a hips in pre-term infants than in full-term
infants. Partenheimer et al23 reported that 6.1% of pre-
term infants had DDH, which was relatively high, however,
the limited size of the study group (n = 33) may have influ-
enced the result.
Various studies have attributed the better maturity of the
hip in premature infants to lower birth weight and intrau-
terine compression.20,24,25 Based on ultrasound scans of the
hip performed in the intrauterine period, Stiegler et al26
showed that the hip reaches maturity according to ultra-
sound criteria in the 34th week of gestation. The maturity
of the hip of the pre-term infants in our study shows that
development of the hip is favourably influenced in the post-
natal period.
We acknowledge the limitations of our study. Although
the sample size was not small, we were unable to evaluate all
infants who were born during the study period. In addition,
all physical and US assessments were performed by a single
physician (MMO) with no assessment of reproducibility.
The most important finding of the study was the signifi-
cantly lower rate of immature hips in pre-term infants
(p < 0.001), whereas the incidence of pathological hips in
the two groups was similar. These findings suggest that pre-
maturity is not a predisposing factor for DDH.
Author contributions:
M. M. Orak: Study design, Writing the paper, Data collection, Data analysis.
T. Onay: Study design, Writing the paper, Data analysis.
S. A. Gümüştaş: Writing the paper, Literature review.
T. Gürsoy: Data collection, Literature review.
H. H. Muratlí: Supervision, Data analysis.
No benefits in any form have been received or will be received from a commer-
cial party related directly or indirectly to the subject of this article.
This article was primary edited by G. Scott and first proof edited by J. Scott
720 M. M. ORAK,T. ONAY, S. A. GÜMÜŞTAŞ, T. GÜRSOY, H. H. MURATLÍ
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