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CME
Article
Abnormal Number of Fetal Ribs on
3-Dimensional Ultrasonography
Associated Anomalies and Outcomes
in 75 Fetuses
Liat Gindes, MD, Bernard Benoit, MD,
Dolores H. Pretorius, MD, Reuwen Achiron, MD
Objective. The purpose of this study was to describe the clinical importance of an abnormal number
of fetal ribs. Methods. A retrospective study of all fetuses that were found to have an abnormal number of ribs during routine ultrasonographic examinations was performed. Volume data sets of the fetal
ribs were acquired by either static 3- or 4-dimensional volume contrast imaging in plane C. In all cases,
a meticulous survey of the fetal anatomy was performed, and prenatal and postnatal records were
reviewed. Results. Seventy-five fetuses were found retrospectively to have an abnormal number of
ribs. Ultrasonographic examinations were done between 14 and 31 weeks’ gestation (mean, 21.8
weeks; median, 23 weeks). More than 24 ribs were found in 28 fetuses (37%), and fewer than 24 ribs
were found in 47 (63%). Additional anomalies were found in 22 fetuses (29%). Cardiovascular
anomalies were detected in 10 fetuses. Seven fetuses had renal anomalies. Two fetuses had mild ventriculomegaly, and 1 fetus had holoprosencephaly. Lung dysplasia was found in 2 cases. One fetus had
enlarged nuchal translucency with wormian bones. Termination of pregnancy was performed in 3
cases because of major malformations. The other 19 fetuses with associated abnormalities and the 53
without associated anomalies were born alive with only minor anomalies. Conclusions. An abnormal
number of fetal ribs is an isolated finding in most cases. It may also be seen with major anomalies;
however, more frequently the anomalies are minor, and the overall prognosis is good. Key words: fetal
skeleton; fetus; ribs; 3-dimensional ultrasonography.
Abbreviations
3D, 3-dimensional; 3DUS, 3-dimensional ultrasonography;
VCI-C, volume contrast imaging in plane C
Received February 4, 2008, from the Department of
Obstetrics and Gynecology, Sheba Medical Center
(Affiliated with the Sackler School of Medicine,
Tel-Aviv University), Ramat Gan, Israel (L.G., R.A.);
Department of Obstetrics and Gynecology,
Princess Grace Hospital, Monaco (B.B.); and
Department of Radiology, Thornton Hospital,
University of California, San Diego, California USA
(D.H.P.). Revision requested February 19, 2008.
Revised manuscript accepted for publication May
13, 2008.
Address correspondence to Liat Gindes, MD,
Department of Obstetrics and Gynecology, Sheba
Medical Center, Tel-Hashomer, 52621 Ramat Gan,
Israel.
E-mail: gindesl@zahav.net.il
CME
Article includes CME test
F
etal rib anomalies have mainly been reported
in association with spondylothoracic dysostosis,
which is a severe fetal deformation that has been
identified during prenatal 2-dimensional ultrasonographic examinations.1,2 New 3-dimensional (3D)
technology allows assessment of in utero fetal rib morphologic and pathologic characteristics.3–5 Case reports
of abnormal ribs shown on 3-dimensional ultrasonography (3DUS) in association with spondylothoracic or
spondylocostal dysostosis have also been reported.3,5,6 To
our knowledge, no data regarding the ultrasonographic
demonstration of the number of fetal ribs have been
reported. A recent case report emphasized the association of an abnormal number of fetal ribs and trisomy 21;
© 2008 by the American Institute of Ultrasound in Medicine • J Ultrasound Med 2008; 27:1263–1271 • 0278-4297/08/$3.50
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Abnormal Number of Fetal Ribs on 3-Dimensional Ultrasonography
however, the exact importance of an abnormal
number of ribs is not known.7 In utero assessment of fetal ribs for number, size, and shape is
important because skeletal dysplasia and genetic, metabolic, infectious, and neoplastic diseases
may occur with rib anomalies.8 The aim of
this study was to review our experience with an
abnormal number of fetal ribs, to correlate it with
clinical outcomes, and to show how to optimally
display the ribs with 3DUS.
Materials and Methods
A retrospective survey of all cases with an abnormal number of ribs that were recorded in 2 diagnostic imaging centers in Israel (Sheba Medical
Center) and Monaco (Princess Grace Hospital) was
performed. Most of the ultrasonographic examinations were performed as a part of standard prenatal care in Israel and Monaco. Approximately 20%
of studies performed in the Sheba clinic had rib
volumes acquired for evaluation because we were
learning how to evaluate the ribs; volumes were
acquired when the fetus was in an adequate position (spine up) and when time permitted. A log was
kept of fetuses with an abnormal rib count.
Examinations were performed during the early
second trimester at 14 to 16 weeks’ gestation or at
22 to 24 weeks’ gestation; 6 fetuses were scanned
outside these periods, and 4 of them had anomalies. Five fetuses were scanned twice during pregnancy. The volumes were evaluated during the
original clinical examination by the same person
who did the study, and all examiners were experienced in 3DUS. The 3DUS protocol was approved
by the Local Committee for Research Ethics at the
Sheba Medical Center; patients in Monaco gave
oral consent to have their data used for research.
All patients had a detailed ultrasonographic examination, and all findings were recorded in an electronic medical file. Fetuses with an abnormal
number of ribs were recorded in a log. Neonatal
data were collected from medical records after
delivery. No routine neonatal chest radiographic
examinations were performed to assess rib numbers; radiographic examinations were done only
for clinical indications.
Studies were performed with commercially
available ultrasound equipment (Voluson 730
Expert; GE Healthcare, Kretztechnik, Zipf, Austria)
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using volumetric abdominal RAB 4-8 and volumetric transvaginal RIC 5-9 transducers. Data sets
of the fetal ribs were acquired either with static 3D
volumes using the skeleton map or with volume
contrast imaging in plane C (VCI-C) using the
spine map. The skeleton map of static 3D volumes
uses a 30% surface mode and a 70% maximum
intensity mode with the low threshold set at 75.
Static 3D volumes were taken with a sagittal
sweep over the fetal thorax and abdomen and
displayed in the anteroposterior projection as
shown in Figure 1. The sweep angle depended on
the gestational age of the fetus and the distance
between the fetus and the transducer. Volumes
were stored and subsequently analyzed on an
offline personal computer with 4D View software
version 5.0 (GE Healthcare). For optimizing the
image volumes, manipulations were performed
by positioning the rendering box, adjusting the
reference plane, and selecting the proper contrast curve for further optimizing the image.
The thickness of the VCI-C technique varied
between 1 and 50 mm; we generally use a thickness of 20 mm. The spine was lined up in the
sagittal plane, and the locator line was positioned
along the spine (Figure 2). The VCI-C display with
the spine map used a 100% maximum intensity
mode with the low threshold set at 20.
Ribs were counted by annotating the image with
a number adjacent to each rib, noticing its position adjacent to paired posterior elements of the
spine. We were not able to determine whether the
extra rib was a cervical rib or lumbar rib. We could
not identify the seventh cervical vertebra.
We could not ascertain the incidence of rib
abnormalities in the general fetal population. We
counted ribs in only a fraction of the fetuses
scanned in our clinics: in prone fetuses that were
positioned with their spine toward the transducer and only when the fetuses were examined by
one of the authors, ie, not when scanned by other
physicians in the ultrasound unit.
Results
From August 2004 to August 2007, 75 fetuses
with an abnormal number of ribs were detected.
More than 24 ribs were found in 28 fetuses
(37%), and fewer than 24 ribs were found in 47
(63%) (Figure 3). In the group with more than 24
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ribs, 20 fetuses (71%) had symmetric ribs: 18 had
13 pairs of ribs (Figure 1B), and 2 had 14 pairs
(Figure 4). Asymmetric ribs in this group were
Figure 1. Thirteen ribs at 23 weeks’ gestation. A, Multiplanar
mode. B, Rendering mode at its maximal setting. The volume
was acquired with the fetus in a sagittal orientation (top left
image). Note that the rendering box is narrow, and the green
line is placed through the posterior elements.
A
found in 8 cases (Figure 5A); all had 13 ribs on one
side and 12 on the other side. In the group with
fewer than 24 ribs, 33 fetuses (70%) had asymmetric ribs (Figure 5B): 32 had 11 ribs on one side
and 12 on the other side, and 1 had 10 ribs on one
side and 11 on the other side. Eleven symmetric
pairs of ribs were seen in 14 fetuses. Fewer than
24 ribs tended to be more asymmetric, and more
than 24 ribs tended to be more symmetric (statistically significant: χ21 = 12.3; P = .0001).
The number of ribs at 15 weeks was less than at
22 to 24 weeks in 5 fetuses. All of these fetuses had
additional ribs on the follow-up scans. Three
fetuses had 12 pairs at 15 weeks that became symmetric (13 pairs) in 1 case and asymmetric (13
and 12) in 2 cases. Two fetuses had asymmetric
ribs (11 and 12) at 15 weeks that became normal
12 pairs at 22 to 24 weeks. All fetuses with an
abnormal number of ribs at 15 weeks’ gestation
were invited for reexaminations at 22 to 24 weeks.
B
Figure 2. Thirteen ribs at 23 weeks’ gestation acquired with
VCI-C.
Figure 3. Distribution of fetuses with an abnormal number of
ribs according to number of pairs and symmetry.
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Abnormal Number of Fetal Ribs on 3-Dimensional Ultrasonography
No additional anomalies were identified during
pregnancy or after birth in 53 fetuses (71%).
Twenty-four additional anomalies were found
in 22 (29%; Table 1). Only 1 fetus had multiple
anomalies, ie, renal and cardiac. Cardiovascular
malformations were found in 10 fetuses (13%).
Most them (7 cases) had vascular anomalies. Five
fetuses had an aberrant right subclavian artery,
and 2 had a single umbilical artery. Only 3 fetuses had cardiac defects: 2 with tetralogy of Fallot
and 1 with a ventricular septal defect. Renal
anomalies were found in 8 fetuses (11%): 5 with
pyelectasis, 1 with a double collecting system,
and 2 with a multicystic dysplastic kidney (1 also
had tetralogy of Fallot and a single umbilical
artery). Three fetuses (4%) had central nervous
system anomalies: 2 with mild ventriculomegaly
that resolved later and 1 with holoprosencephaly.
Bronchopulmonary dysplasia was found in 2
fetuses (2.7%): 1 with sequestration and 1 with a
congenital cystic adenomatoid malformation.
Figure 4. Fourteen symmetric pairs of ribs on a rendered image
taken from a 3D static volume.
One fetus (1.3%) had enlarged nuchal translucency of 4 mm with wormian bones.
Karyotypes were obtained in 28 patients (37%)
and were found to be normal in all of them. Three
patients elected to terminate pregnancy, all with
a normal karyotype. One fetus had holoprosencephaly; 1 had increased nuchal translucency,
lateral neck cysts, and wormian bones; and 1 had
tetralogy of Fallot, a multicystic dysplastic kidney, and a single umbilical artery. All 72 fetuses
that continued to birth were alive and well and
were not found to be dysmorphic on pediatric
examinations.
Only 3 neonates had chest radiography after
delivery: 1 for bronchopulmonary sequestration
(Figure 6) and 2 by maternal request. The prenatal diagnosis of an abnormal number of ribs was
confirmed in all 3 cases.
Patient counseling when imaging studies
showed an abnormal number of fetal ribs included the following: (1) in cases of an isolated finding, patients were told that it was most probably
a variation of normal; (2) detailed explanations of
the limitations of the study were provided to
patients; (3) counseling was given according to
the additional anomalies that were found; and
(4) genetic counseling and risk calculation for trisomy 21 were recommended.
In the cases with an isolated finding of an
abnormal number of ribs, the prenatal care was
not changed. We asked the patients to inform the
neonatologist of the abnormal rib findings after
delivery.
Discussion
The finding of an abnormal number of fetal ribs
can be incidental or can be associated with
major congenital anomalies that may influence
parental decisions regarding continuation of
pregnancy. Although information regarding an
abnormal number of ribs is available from the
neonatal/pediatric literature, it is important to
recognize that fetuses are not small children and
that fetuses with major abnormalities often do
not make it into the neonatal literature because
of fetal death or termination of pregnancy.
Although an abnormal number of ribs has been
described in individuals with genetic diseases
(Poland syndrome, VATER [vertebral anomalies,
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anal atresia, cardiovascular anomalies, tracheoesophageal fistula, esophageal atresia, renal or
radial anomalies, and limb anomalies], cleidocranial dysplasia, and campomelic dysplasia),
scoliosis and segmentation anomalies of the vertebrae, and abnormal karyotypes (Table 2), none
of the cases in this study showed these associations.7–10 It has been reported that the incidence
of 11 rib pairs in neonates with trisomy 21 is 28%
to 33%.7,15 This study examined the clinical
importance of an abnormal number of fetal ribs
identified in utero.
Normally there are 12 pairs of ribs that develop
from cartilaginous costal processes of the developing thoracic vertebrae.16 They become cartilaginous during the embryonic period and ossify
during the fetal period. The upper 7 pairs are
attached anteriorly to the sternum by their costal
cartilages. The 8th, 9th, and 10th pairs of ribs are
attached anteriorly to each other and to the 7th
rib by means of their costal cartilages and small
synovial joints. The 11th and 12th pairs have no
anterior attachment and are referred to as floating ribs. The ossification process is completed at
puberty.17
The best imaging of fetal ribs is obtained with
static 3D volumes in a sagittal sweep when the
fetus is at rest with the back toward the transducer. When the fetus is moving, the thick-slice
method (VCI-C) is more beneficial. The maximal
mode rendering map displays the fetal ribs best.
It is important to take volumes when the back is
symmetric on both sides to prevent acoustic
shadowing, which can lead to the suspicion of an
absent rib. Several cervical vertebral bodies and
several lumbar vertebral bodies should be
Figure 5. Asymmetric number of ribs. A, more than 24 (12 and 13) at 14 weeks’ gestation. B, Fewer then 24 (11 and 12) at 23
weeks. Each image was taken from a 3D static volume.
A
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B
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Abnormal Number of Fetal Ribs on 3-Dimensional Ultrasonography
Table 1. Additional Malformations
System
Cardiovascular
Malformations, n (%)
10 (45)
Renal
8 (36)
CNS
3 (14)
Lung
2 (9)
Other
1 (5)
Pathologic Findings
Fetuses, n
ARSA
SUAa
TOFa
VSD
Pyelectasis, mild
MCDKa
Double collecting system
Ventriculomegaly, mild
Holoprosencephaly
Sequestration
CCAM
Wormian bone and abnormal NT
5
2
2
1
5
2
1
2
1
1
1
1
Remarks
1 TOP
TOP
TOP
ARSA indicates aberrant right subclavian artery; CCAM, congenital cystic adenoid malformation; CNS, central nervous
system; MCDK, multicystic dysplastic kidney; NT, nuchal translucency; SUA, single umbilical artery; TOF, tetralogy of Fallot;
TOP, termination of pregnancy; and VSD, ventricular septal defect.
a
One fetus had 3 malformations.
included in the volume to prevent miscounting
fewer ribs than exist. The ability to distinguish
between cervical, thoracic, and lumbar ribs is
limited, especially in the coronal plane. The cervical rib has a different shape in the axial plane,
but more research is needed to identify a cervical
rib accurately in the fetus.
We have reviewed 75 fetuses with an abnormal
number of ribs; 37% of them had supernumerary
ribs, and 63% had subnumerary ribs. This is similar to the work of Merks et al,13 who reported the
incidence of an abnormal number of ribs in a
pediatric population of healthy white children
as 13.6% (120 of 881) and that in children with
childhood cancer as 13.7% (125 of 906); half of
the cases had supernumerary ribs, and half had
subnumerary ribs. From our study, it was not
possible to obtain the true incidence of abnormal ribs in the general population because our
study was a retrospective case collection.
Figure 6. Eleven symmetric pairs of ribs at 22 weeks’ gestation.
A, Three-dimensional sonogram. B, Neonatal chest radiograph.
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The literature that focused on abnormalities of
the ribs in the neonatal period related them to
generalized skeletal disorders and genetic and
metabolic diseases.9 Until recently, fetal rib
anomalies were mainly described in association
with severe fetal malformations.3,7 Hull et al3 were
the first to report the use of a 3D technique in a
severe case of spondylothoracic dysostosis. None
of our fetuses had severe spondylocostal dysostosis, which is a rare congenital disorder characterized by short-trunk dwarfism associated with rib
and vertebral anomalies.5 Benoit4 described the
use of 3D imaging in evaluation of the fetal skeleton. He suggested that 3DUS is the investigation
tool of choice for studying the fetal skeleton at
any time during gestation. He showed that the
posterior view of the fetus gives good access to the
spine and allows the ribs to be counted correctly.
These techniques can also be used to evaluate
fetuses at risk of structural rib abnormalities.
Hypoplasia of the 12th rib was recently
described by Esser et al7 using 3DUS in a fetus
with trisomy 21. The ribs are well known to be
involved in trisomy 21 in children: 11 rib pairs
were reported in 28% of children with trisomy 21
(14 of 50) and 4% of unaffected children (8 of
200).15 In 1988, Edwards et al10 reported 11 rib
pairs in 33% of neonates with trisomy 21 (10 of
30) and 5% of unaffected children (46 of 881), a
6.6 times higher incidence. In this study, 14 fetuses had 11 pairs of ribs; only 1 had a major malformation, but the fetus had a normal karyotype.
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Table 2. Pathologic Findings Associated With an Abnormal Number of Ribs According to the Literature
Ribs
Pathologic Findings
References
7 pairs
11
Trisomy 21, cleidocranial dysplasia, camptomelic dysplasia
Trisomy 18, 21
Childhood malignancy
Trisomy 21
VATER
Monosomy X
Acute lymphoblastic leukemia, astrocytoma and germ cell tumor,
neuroblastoma, brain tumor, soft tissue sarcoma, Wilms tumor,
Ewing sarcoma
Spondylocostal dysostosis
Glass et al8
Glass et al,8 Hannam et al,9 Edwards et al10
Loder et al11
Glass et al,8 Edwards et al10
Glass et al8
Keeling et al12
Merks et al,13 Schumacher et al14
13
14
Cervical rib
Asymmetric rib
anomalies
del Rio et al,1 Hull et al,3 Wong et al5
VATER indicates vertebral anomalies, anal atresia, cardiovascular anomalies, tracheoesophageal fistula, esophageal atresia, renal or radial anomalies, and limb anomalies.
A fetal karyotype examination is not a routine procedure; however, 37% of the 75 patients in this
study elected to have a karyotype examination
performed from amniocentesis during gestation,
and all were normal. None of the 72 fetuses that
were born showed any genetic dyspmorphism. The
minor anomalies were confirmed after delivery by
neonatal ultrasonography and echocardiography.
We did not have follow-up beyond the neonatal
period. A larger prospective cohort study is needed to evaluate the added risk of trisomy 21 in
fetuses with an abnormal number of ribs.
We have found that 29% of our population (22
of 75) showed a diverse group of additional
anomalies; only 3 patients (4%) terminated pregnancy: 2 because of severe fetal anomalies and 1
because of uncertainty regarding the outcome.
Overall, in 96% of our cases the prognosis was
excellent, and all fetuses were born healthy and
alive. The most common anomalies observed in
our study were vascular, followed by renal and
lung anomalies (Table 1). An aberrant right subclavian artery was identified in 5 fetuses in our
study; Chaoui et al18 reported an association of
that finding with Down syndrome (5 of 14 fetuses with Down syndrome had an aberrant right
subclavian artery), but our numbers were too
small to find this association. The presence of
minor anomalies in fetuses with rib anomalies
emphasizes the need for a meticulous examination in each fetus in whom abnormal ribs are
detected on ultrasonography.
J Ultrasound Med 2008; 27:1263–1271
Chest radiography was not performed to
confirm the prenatal findings in our patient
population because of medical and ethical
considerations. Three patients had chest radiography, and an abnormal number of ribs was
confirmed: 1 with bronchopulmonary sequestration and 2 by maternal request (Figure 6). The
accuracy of the findings cannot be compared to
a reference standard such as chest radiography
but can be compared to the quality of the ultrasonographic volume and repeated counting in
several volumes from the same fetus.
An interesting finding in our study was the
observation of the changing numbers of ribs
from an early scan at 15 weeks to a later scan.
Because in all cases the end result was an additional rib on follow-up, we speculate that
either the additional rib was underossified or
hypoplastic on the first scan. Whatever the reason, we suggest informing patients about this
observation if an abnormal number of ribs is
identified. Postponing rib counting to later in
pregnancy will prevent this mistake; however, it
may also prevent early detection of additional
anomalies.
The epidemiologic association between childhood malignancies and an abnormal number of
ribs has recently been reported. Two European
studies and 1 American study reported this association.11,13,14 Each study found that fewer than
24 ribs and cervical ribs have an association
with pediatric malignancies. Schumacher et al14
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reviewed 1000 chest radiographs of children with
malignancies and compared them to 200 chest
radiographs of children with mainly infectious
diseases. They found rib anomalies in 21.8% of
the study group and 5.5% of the control group.
Merks et al13 studied chest radiographs of 881
white pediatric control patients (patients with
asthma and infectious diseases) and 906 patients
with childhood cancer. They looked for rib
anomalies and found an abnormal number of
ribs in 13.7% and 13.6% of the cancer and control
groups, respectively. Their control group was
not ideal, and they found a high incidence of rib
anomalies in both groups. Loder et al11 retrospectively reviewed 218 children with malignancy and 200 control patients with polytrauma or
suspected child abuse. They found an abnormal
number of ribs in 8% of the control group and
17.9% of the study group. These reports discussed
the relationship between rib anomalies and
malignancy. The homeobox genes are important in the development of the axial skeleton,
and abnormalities in those genes are also associated with malignancies. Whether an abnormal
number of ribs can be used as a predictor of
malignancy will require additional research.
Meanwhile, we do not think that this information
should be used to alarm parents regarding an
increased risk of malignancy in their fetuses.
The limitations of this study included the following. First, the incidence of an abnormal number of fetal ribs could not be measured from this
study. There was a selection bias in our study
population. We were unable to study all fetuses,
and this would be necessary to assess the risk of
trisomy 21. Second, the true reference standard
would be pathologic counting of the ribs, which
is not possible. Even chest radiographs cannot
always provide this information. Also, comparison of our results to chest radiographic findings
would not be ethical. Third, in our study we were
not able to delineate whether the supernumerary
rib was a cervical rib or a lumbar rib. Our imaging
techniques only allowed the posterior aspect of
the fetal chest to be visualized.
In summary, an abnormal number of fetal ribs
is often associated with minor abnormalities
(29% in our study) and only occasionally with a
severe malformation. However, a thorough organ
investigation to exclude malformations is recom1270
mended. The role of genetic amniocentesis
should be considered for each case on the basis
of its individual risk assessment. Generally, the
prognosis in these cases is favorable, and a larger
prospective study should be performed to assess
the incidence and calculated additional risk of
genetic and other malformations.
References
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del Río Holgado M, Martínez JM, Gómez O, et al.
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Eliyahu S, Weiner E, Lahav D, Shalev E. Early sonographic
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Hull AD, James G, Pretorius DH. Detection of Jarcho-Levin
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4.
Benoit B. The value of three-dimensional ultrasonography
in the screening of the fetal skeleton. Childs Nerv Syst
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5.
Wong GY, Wong SF, Chan WP, Ng WF. Three-dimensional
ultrasound findings of spondylocostal dysostosis in the second trimester of pregnancy. Ultrasound Obstet Gynecol
2006; 27:580–582.
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Sallout B, D’Agostini D, Pretorius D. Prenatal diagnosis of
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7.
Esser T, Rogalla P, Sarioglu N, Kalache K. Three-dimensional ultrasonographic demonstration of agenesis of the 12th
rib in a fetus with trisomy 21. Ultrasound Obstet Gynecol
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Glass RB, Norton KI, Mitre SA, Kang E. Pediatric ribs: a
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Hannam S, Greenough A, Karani JB. Rib abnormalities arising before and after birth. Eur J Pediatr 2000; 159:264–
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Loder RT, Huffman G, Toney E, Wurtz LD, Fallon R.
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Keeling JW, Kjaer I. Cervical ribs: useful marker of monosomy X in fetal hydrops. Pediatr Dev Pathol 1999; 2:119–
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Merks JH, Smets AM, Van Rijn RR, et al. Prevalence of rib
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Beber BA, Litt RE, Altman DH. A new radiographic finding
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Moore KL, Persaud TVN (eds). The skeletal system. In: The
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Fitzgerald MJT (ed). Spinal cord and body wall. In: Human
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Chaoui R, Heling KS, Sarioglu N, Schwabe M, Dankof A,
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