Cranial Ultrasound as a First- Line Imaging Examination ......for evaluation of the cranial sutures...
Transcript of Cranial Ultrasound as a First- Line Imaging Examination ......for evaluation of the cranial sutures...
ARTICLEPEDIATRICS Volume 137 , number 2 , February 2016 :e 20152230
Cranial Ultrasound as a First-Line Imaging Examination for CraniosynostosisKatya Rozovsky, MD,a,b Kristin Udjus, MD,a Nagwa Wilson, MD, PhD,a Nicholas James Barrowman, PhD,c Natalia Simanovsky, MD,b Elka Miller, MDa
abstractBACKGROUND: Radiography, typically the first-line imaging study for diagnosis of
craniosynostosis, exposes infants to ionizing radiation. We aimed to compare the
accuracy of cranial ultrasound (CUS) with radiography for the diagnosis or exclusion of
craniosynostosis.
METHODS: Children aged 0 to 12 months who were assessed for craniosynostosis during
2011–2013 by using 4-view skull radiography and CUS of the sagittal, coronal, lambdoid,
and metopic sutures were included in this prospective study. Institutional review board
approval and parental informed consent were obtained. CUS and radiography were
interpreted independently and blindly by 2 pediatric radiologists; conflicts were resolved
in consensus. Sutures were characterized as closed, normal, or indeterminate. Correlation
between CUS and radiography and interreader agreement were examined for each suture.
RESULTS: A total of 126 children (82 boys, 64.5%) ages 8 to 343 days were included. All
sutures were normal on CUS and radiography in 115 patients (93.7%); craniosynostosis
of 1 suture was detected in 8 (6.3%, 5 sagittal, 2 metopic, 1 coronal). In 3 cases the
metopic suture was closed (n = 2) or indeterminate on CUS (n = 1) but normally closed on
radiography. CUS sensitivity was 100%, specificity 98% (95% confidence interval 94%–
100%). Reader agreement was 100% for sagittal, coronal, and lambdoid sutures (κ = 0.80);
after consensus, disagreement remained on 3 metopic sutures.
CONCLUSIONS: In this series, CUS could be safely used as a first-line imaging tool in the
investigation of craniosynostosis, reducing the need for radiographs in young children.
Additional assessment may be required for accurate assessment of the metopic suture.
aDepartment of Medical Imaging, and cResearch Institute, Children’s Hospital of Eastern Ontario, University of
Ottawa, Ottawa, Ontario, Canada; and bDepartment of Diagnostic Imaging, Hadassah-Hebrew University Medical
Center, Jerusalem, Israel
Dr Rozovsky conceptualized and designed the study, and drafted the initial manuscript; Drs
Udjus and Wilson recruited patients, supervised the cranial ultrasound studies, contributed to
data acquisition, and reviewed and revised the manuscript; Mr Barrowman designed the data
collection instruments, provided statistical analyses, and critically reviewed the manuscript;
Dr Simanovsky contributed to the conception and design of the work, and reviewed and revised
the manuscript; Dr Miller contributed to the conception and design of the work, to acquisition,
analysis, or interpretation of data, and critically reviewed the manuscript; and all authors
approved the fi nal manuscript as submitted.
DOI: 10.1542/peds.2015-2230
Accepted for publication Nov 16, 2015
To cite: Rozovsky K, Udjus K, Wilson N, et al. Cranial
Ultrasound as a First-Line Imaging Examination for
Craniosynostosis. Pediatrics. 2016;137(2):e20152230
WHAT’S KNOWN ON THIS SUBJECT: In many
pediatric practices, the fi rst-line imaging modality
for evaluation of the cranial sutures is a 4-view
cranial radiograph. Cranial ultrasound is an
alternative technique for diagnosis or exclusion
of craniosynostosis that is radiation-free and
technically simple.
WHAT THIS STUDY ADDS: In young children referred
for evaluation of the cranial sutures, we found that
cranial ultrasound could replace radiography as the
fi rst-line imaging study for diagnosis or exclusion
of craniosynostosis, reducing exposure to ionizing
radiation in this vulnerable population.
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
ROZOVSKY et al
Craniosynostosis, defined
as the premature closure
of ≥1 cranial sutures, is the most
frequent craniofacial anomaly,
occurring in 4 to 6 infants
per 10 000 live births.1–3
Craniosynostosis can present as an
isolated finding or in association
with various syndromes. Although
an isolated single cranial suture
closure usually causes only cosmetic
deformity,1 poor gross motor
function and learning difficulties
resulting from even a single suture
synostosis have been reported.4–7
Multiple suture synostosis, usually
syndromic, has been associated
with several complications,
such as increased intracranial
pressure, headaches, and delayed
neurodevelopment.8
The initial imaging study for infants
with suspicion of this condition is
generally 4-view radiography9–13
followed by computed tomography
(CT) in cases of positive or equivocal
findings at radiography. CT with
3-dimensional reconstruction
delineates the diagnosis and guides
preoperative management.2,9,12,14
Cranial ultrasound (CUS) is an
alternative imaging modality that is
underused in this context. It offers
excellent imaging of superficial
structures with the potential to
confirm or exclude fusion of cranial
sutures while avoiding exposure to
ionizing radiation in the very young
infant. The normal gap of a patent
suture (Fig 1) or the obliteration
in craniosynostosis can be clearly
demonstrated with CUS in children
<12 months of age.15–21
Data in previous publications support
CUS as an easy and feasible imaging
technique for assessment of the cranial
sutures. In recent study by Linz et al,22
CUS confirmed a clinical diagnosis of
craniosynostosis or plagiocephaly in
large group of infants.
Most studies have compared CUS
with CT and have successfully
demonstrated the accuracy of
CUS for the detection or exclusion
of craniosynostosis.16,18,19,21,23,24
The lack of a larger series
comparing findings of CUS with
plain radiographs in this setting
may be partly responsible for the
underutilization of CUS as a first
imaging tool for the detection of
craniosynostosis.
We aimed to determine whether
CUS could replace radiography for
the detection of craniosynostosis.
The specific objective of this
prospective study was to compare
the accuracy (sensitivity and
specificity) of CUS (index test) versus
radiography (reference standard)
for the diagnosis or exclusion of
craniosynostosis.
METHODS
Institutional review board approval
and written informed consent from
2
FIGURE 1Sonographic anatomy of a cranial suture. The fi gure was created based on sonographic-histologic correlation, provided by Soboleski et al.19 Transverse sonogram of coronal suture demonstrates hypo echogenic gap (horizontal arrow) between hyper echogenic bony plates of the skull (diamond shapes). Asterisk indicates soft tissues of the scalp. Solid arrowhead points to the thin line of dural interface.
FIGURE 2Flowchart of the study.
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
PEDIATRICS Volume 137 , number 2 , February 2016
parents or guardians were obtained
for this prospective study.
Subjects
Consecutive patients aged 0 to
12 months who were referred to
the Children’s Hospital of Eastern
Ontario, Ottawa, Canada, from
March 2011 to September 2013
for radiographic evaluation due
to a suspicion of craniosynostosis
were eligible for inclusion. On
presentation to the department, a
researcher (E.M., K.R., K.U., N.W.)
approached the parent or guardian
before radiographs were obtained
for consent to perform CUS. Children
were excluded if their parent or
guardian did not consent or if CUS
images were suboptimal due to poor
cooperation.
Imaging Protocols
The order of imaging was always
radiography first and then CUS.
Anterior-posterior Caldwell, anterior-
posterior Towne, lateral, and
submentovertical skull radiographs
were obtained as per departmental
protocol (kV 77, mAs 1.0–2.0
depending on patient size and
density; Digital Diagnostic, Philips
HealthCare, Eindhoven, Netherlands).
All 5 departmental sonographers
had been previously trained by 2
radiologists (K.R., E.M.) for CUS
assessment of the cranial sutures by
using the cranial suture simulator
model recommended by Ngo et
al.25 A senior radiologist with 5 to
25 years of experience in pediatric
ultrasound studies was present
during the entire CUS (E.M., K.R., K.U.,
N.W.). Radiologists, sonographers,
and family members were blinded to
the findings at radiography during
the CUS examination.
CUS was performed by using a
12-MHz linear transducer (IU22
Image System; Phillips HealthCare)
with the child placed supine or in a
semisitting position on a parent’s
lap, with the head mildly tilted for
3
FIGURE 3Assessment of the cranial sutures in a 7-month-old boy, referred to exclude craniosynostosis. A–F: CUS demonstrated normal sagittal, right and left coronal, right and left lambdoid, and metopic sutures (arrows). Note the absence of a hypoechoic gap for the metopic suture. This is the characteristic appearance of a normally closed metopic suture.
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
ROZOVSKY et al
optimal sonographic penetration.
The CUS study focused solely on
evaluation of the sagittal, coronal,
lambdoid, and metopic sutures.
The transducer was oriented
perpendicular to the long axis of the
suture being examined, along its
entire course. The metopic suture
was scanned between the frontal
bones, limited posteriorly by the
anterior edge of the anterior fontanel.
The sagittal suture, which divides
the right and left parietal bones, was
scanned from the posterior edge of
the anterior fontanel to the anterior
edge of the posterior fontanel. The
left and right coronal and lambdoid
sutures were scanned from the
midline (lateral edges of the anterior
fontanel for coronal sutures and
posterior fontanel for lambdoid
sutures) to the periphery. Total CUS
time was ≤20 minutes. CUS images
were recorded and stored in the
picture archiving and communication
system (PACS) system as a research
study with a unique research study
number.
Image Interpretation Protocol
To standardize the approach,
5 randomly chosen studies
(radiographs and CUS) were
interpreted in consensus by 2
pediatric radiologists (E.M., K.R.,
11 and 7 years of experience,
respectively) during data acquisition.
Approximately 3 months after
closure of data acquisition, the
same 2 radiologists independently
interpreted all radiography and CUS
studies. The readers were blinded
to clinical indications and previous
reports. During the review, all the
CUS studies were interpreted first,
before radiography studies, to ensure
that the radiographic images would
not influence interpretation of CUS.
Discrepancies between readers were
resolved in consensus.
Findings were documented on the
hospital’s Research Electronic Data
Capture (REDCap) system (REDCap
Consortium, http:// www. project-
redcap. org/ ).
Qualitative Interpretation
CUS and radiographic examinations
were categorized for each suture as
normal (hypoechoic gap between
the bones, equivalent to patent
suture), closed (no hypoechoic gap
between the bones, suggestive of
bridging or bone deformation), or
indeterminate. Because physiologic
closure of the metopic suture occurs
during the first year, the definition of
a “normal” metopic suture included
either patent (when a hypoechoic
gap was present) or normally closed
(absence of a hypoechoic gap with no
ridging of the sutures in children >3
months of age). Craniosynostosis was
defined as the presence of at least 1
abnormally closed suture.
Comparison of CUS to CT
A small number of CT studies that
had been performed for study
participants were identified and
reviewed by the readers only after
all CUS and radiographs had been
interpreted.
Statistical Analysis
With radiography as the reference
standard, the sensitivity and
specificity of CUS were computed
using the Wilson score method.
The extent of agreement between
readers on qualitative assessment
of suture patency on radiographic
and CUS studies was evaluated
by using the Cohen unweighted κ.
Statistical analyses were performed
by using SPSS (IBM SPSS Statistics
for Windows, version 22.0; IBM
Corp, Armonk, NY) and R version
3.1.0 (R Core Team, R Foundation
for Statistical Computing, Vienna,
Austria).
RESULTS
Subjects
Among 150 consecutive patients
evaluated by radiography, 21 parents
did not consent to the CUS study,
either because the parents did not
have time to wait for the study or
were reluctant to expose the infant
to further medical examinations.
From the 129 consented children
who underwent CUS, 3 patients were
excluded because their studies were
suboptimal due to poor cooperation
4
FIGURE 4A, Cranial radiography, frontal view, in the same patient. The lambdoid sutures are not clearly seen in this view, which prompted the referring physician to request CT evaluation. B, Three-dimensional reconstruction of cranial CT revealed a normally closed metopic suture and patent sagittal, coronal, and lambdoid sutures.
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
PEDIATRICS Volume 137 , number 2 , February 2016
of the child (9-month-old girl,
7-month-old-girl, 10-month-old boy).
The study group thus included 126
patients (male-to-female ratio, 82:44;
mean age 168.4 ± 2.7 days, range
8–343 days, or 5.5 months, range
0.26–11.27 months) (Fig 2).
Clinical indications for radiography
included small or prematurely closed
fontanels (51 patients), suspected
closed lambdoid sutures/plagiocephaly
(right side 14 patients, left side 9,
unspecified side 23), suspected
closed sagittal suture (7 patients),
closed coronal suture (right side
5 patients, left side 5), metopic
synostosis (5 patients), and small
head circumference (4 patients).
In 18 other patients, the indication
provided by the clinician was “rule
out craniosynostosis.” Other indications
included macrocephaly (4 patients),
and bony ridge anterior forehead,
posterior midline bump, septo-optic
dysplasia, genetic syndrome not
yet diagnosed, or neonatal Graves’
disease (1 case for each indication).
Qualitative Suture Assessment on CUS and Radiography
A total of 115 (91.3%) of 126 patients
had normal sutures on both CUS and
radiography studies (Figs 3 and 4).
A single closed suture was depicted
with both imaging modalities in 8
infants (6.3%), including sagittal
sutures in 5 children aged 2.1,
2.2, 3.8, 4.3, and 5.5 months (Fig
5); metopic sutures in 2 children
aged 2.3 and 5.3 months (Fig 6);
and a right coronal suture in 1
child aged 0.5-month (Fig 7). No
cases of multiple suture closure
were detected on either CUS or
radiography.
There was complete agreement
between CUS and radiograph for
the sagittal, coronal, and lambdoid
sutures (κ = 1). In 3 cases there was
disagreement between CUS and
radiographs regarding the status
of the metopic sutures. On CUS
examination, the metopic suture
was found to be closed (synostosis)
in 2 boys aged 8 months old and
indeterminate in an 11-month-old
girl, whereas it was depicted as
normally closed on radiography in
all 3 cases (κ for metopic suture =
0.56) (Fig 2). Overall, CUS sensitivity
was 100%, specificity was 98% (95%
confidence interval 94%–100%).
Interobserver Agreement
Interobserver agreement for the
presence of any closed suture by
CUS was high (κ 0.80). There was
agreement between the readers on
122 (96.8%) of 126 CUS studies.
There was disagreement regarding
the interpretation of the metopic
suture in 4 cases. At consensus
interpretation of the CUS studies,
these metopic sutures were
considered closed normally in 2
cases, closed with synostosis in 1
child (Fig 6), and indeterminate in
1 case. All of these sutures were
considered “normally closed” on
radiography. CT was not performed
in any of the 4 children.
5
FIGURE 5A, A 2-month-old boy with suspected sagittal synostosis. CUS showed obliteration of the normal hypoechogenic gap between the parietal bones, representing an abnormally closed sagittal suture (arrow). B, Frontal cranial radiograph in the same patient confi rms a closed sagittal suture with some sclerosis along the suture (arrow). C, Three-dimensional reconstruction of cranial CT confi rmed abnormal closure of the sagittal suture (arrow).
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
ROZOVSKY et al
There was disagreement in the
interpretation of radiography study
for metopic sutures in 5 patients. All
cases were resolved in consensus,
and the consensus interpretation was
then used as the reference standard
in these cases. In 3 of 5 cases, there
was disagreement in interpretation
of CUS as well.
In 1 girl aged 5 months old, the
metopic suture was considered closed
(synostosis) by 1 reader and “normally
closed” by another on radiography; it
was called as “closed (synostosis)” in
consensus reading. On CUS, the suture
was called “closed (synostosis)” by
both readers. In an 8-month-old boy,
the suture was considered closed
(synostosis) by 1 reader and “normally
closed” by another on radiography; it
was interpreted as “normally closed”
after consensus. The suture was called
“closed (synostosis)” by both readers
on CUS.
Comparison of CUS to CT
Cranial CT was performed in 11
(8.7%) of 126 children at the request
of the referring physician. CT was
performed for surgical planning
in cases in which craniosynostosis
was diagnosed on radiography
(6 children), when there was a
suspicion of synostosis and findings
at radiography were equivocal
(4 children), and in 1 case of
accidental trauma. Findings at CT
were consistent with radiography
and CUS in all 11 cases. In 6 cases
of craniosynostosis (true-positive
cases), there was closure of the
sagittal suture in 4 children (Fig 5),
the coronal suture in 1(Fig 7), and
the metopic suture in 1.
In 5 of 11 infants, the sutures were
normal. The referring physician
requested CT evaluation of the
sagittal and lambdoid suture,
respectively, in a 1.5-month-old
boy and a 9-month-old girl, despite
normal cranial radiography. CT
was ordered for a 7-month-old boy
after right plagiocephaly was seen
on radiography; on CT, the sutures
were normal (Figs 3 and 4). CT was
ordered for a 7-month-old boy with
a small fontanel in spite of negative
radiography and CUS. This CT study
was prompted by the radiologist’s
report of cranial radiograph, which
contained a comment on sclerotic
changes of the metopic suture. The
metopic suture was closed normally
on CT. Another CT was prompted
by an unrelated accidental trauma
in a 5-month-old girl who had
been examined at age 3 months for
suspected premature closure of left
coronal and lambdoid sutures. The
sutures were normal on radiography
and CUS, and remained patent at the
time of the CT.
DISCUSSION
In the current patient series, CUS
performed by sonographers in ≤20
minutes provided good accuracy for
the detection of craniosynostosis
with 100% sensitivity and 98%
specificity (95% confidence interval
94%–100%) in comparison with
4-view radiographs. There was
full agreement in interpretation of
radiography and CUS for the sagittal,
coronal, and lambdoid sutures; there
was disagreement between the 2
studies for assessment of the metopic
suture in 3 of 126 children.
Previous studies evaluating the
accuracy of CUS for evaluation of the
cranial sutures have compared CUS
with CT.15,16,18,19,21,23,24 Regelsberger
et al16 reported 100% success of CUS
in the detection of craniosynostosis
in 26 patients proven to have this
condition on CT. Sze et al24 used CUS
6
FIGURE 6A, A 5-month-old boy was referred to exclude craniosynostosis. CUS of the metopic suture demonstrated a closed, triangularly shaped suture (arrow). B, In agreement, frontal cranial radiograph in the same child showed an abnormally closed metopic suture with bony ridging (arrows) and orbital hypotelorism. Surgical reconstruction was performed (not shown). C, An 8-month-old boy was referred due to suspicion of metopic synostosis. CUS demonstrated a closed, triangularly shaped metopic suture (arrow). D, In disagreement, frontal cranial radiograph in the same child showed an absence of bony ridging and normal distance between the orbits, in keeping with the appearance of a normally closed metopic suture.
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
PEDIATRICS Volume 137 , number 2 , February 2016
for evaluation of the lambdoid suture
in 41 children undergoing CT scan for
suture assessment, and found a mean
sensitivity and specificity of 100%
and 89%, respectively. Houman
Alizadeh et al15 studied 44 children
aged <1 year with a diagnosis of
synostosis, and demonstrated a
sensitivity, specificity, and positive
and negative predictive for CUS
versus CT scan of 96.9%, 100%,
100%, and 92.3%, respectively.
However, to our knowledge, previous
studies have not compared the
accuracy of CUS and radiography
in this setting. Therefore, the
purpose of this study was to take a
step back before CT is considered
and compare findings from cranial
radiographs and CUS in the diagnosis
of craniosynostosis.
In cases in which craniosynostosis is
suspected, an accurate diagnosis is
essential. Although craniosynostosis
is the most frequent craniofacial
anomaly, premature closure of
cranial sutures is an uncommon
condition.1–3 Imaging studies rule
out abnormal suture closure in most
cases. In our study, as expected,
the great majority of children
(93.7%) had a negative radiograph.
However, radiographic studies
expose these very young children,
who are particularly sensitive, to
the deleterious effects of ionizing
radiation.26 Reliance on radiography
in cases in which there is an
alternative imaging technique that
avoids exposure to ionizing radiation
contradicts the principles of “as low
as reasonably achievable” and “image
gently” recommendations.27
To date, ultrasound has not shown
any harmful biological effects in
children and is routinely used for
evaluation of the neonatal brain.
The imaging workup in cases of
suspected craniosynostosis is
affected by referral patterns. In some
centers the diagnostic algorithm
may vary from clinical evaluation
only to the use of different imaging
modalities, depending on the
preferences of referring physicians.
Schweitzer at al28 described their
experience with evaluation of
children with single lamboid suture
craniosynostosis or positional
plagiocephaly. In 133 (97%) of 137
infants, the diagnosis was made
with clinical examination and no
imaging studies were required. In a
recent publication by Linz et al,22 the
diagnosis of positional plagiocephaly
was made by clinical examination
alone in 258 of 261 cases, whereas in
3 children, the final diagnosis became
possible only after CUS examination.
CUS confirmed the clinical diagnosis
in 261 of 261 children with positional
plagiocephaly and in 8 of 8 cases
of lambdoid synostosis. In both of
these studies, the clinical diagnosis
was made by experienced pediatric
neurosurgeons, which should be
7
FIGURE 7A 15-day-old girl was referred for cranial suture evaluation due to plagiocephaly. CUS depicted a closed right coronal suture (B, arrow) with bridging of the bone and a patent left coronal suture at the same level (A, arrow). C, Frontal cranial radiograph in the same patient showed right coronal synostosis with a “harlequin eye” on the right side (arrow). D, Three-dimensional reconstruction of cranial CT confi rmed abnormal closure of the right coronal suture (arrow).
FIGURE 8Recommended algorithm for diagnosis or exclusion of nonsyndromic craniosynostosis by pediatrician or family practitioner.
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
ROZOVSKY et al
the ideal practice. However, in
many places throughout the world,
access to a neurosurgeon is low,
and responsibility for making the
initial diagnosis rests with a family
practitioner or pediatrician.29 In this
setting, imaging studies are essential.
When imaging is key to the diagnosis,
we suggest that CUS may become the
first-line technique, avoiding routine
use of radiography as an initial
examination (Fig 8).
CUS is a short, simple, and
inexpensive study, and may be
performed by ultrasound specialists
with minimal additional training by
an experienced ultrasonographer. In
comparison with skull radiography,
infants are in a more comfortable
position during the CUS studies; they
can sleep or even be fed during the
examination.
In the current study, interpreting
radiologists who blindly and
independently interpreted both
radiography and CUS studies were in
full agreement in their assessments
of the sagittal, coronal, and lambdoid
sutures; however, in 3 cases they
disagreed regarding the status of the
metopic suture. Metopic synostosis
continues to represent a debate in
the radiology and neurosurgery
communities ), and can be difficult
to evaluate as children grow because
this suture normally tends to close
early.30 In contrast to radiographs, a
radiologist performing or supervising
the CUS has the opportunity to
clinical visualize the forehead,
and correlate its appearance on
ultrasound with age of the infant.
The metopic suture is known to
close more rapidly than the other
sutures. Vu et al31 studied the timing
of physiologic closure of normal
metopic sutures in a 159 CT studies.
They reported the earliest evidence of
closure at 3 months of age, and by 9
months the metopic suture was closed
in 100% of the children. In a study
by Weinzweig et al,30 metopic suture
fusion was complete by 6 to 8 months
on CT evaluation. In the current series,
the youngest age for physiologic
fusion of the metopic suture on CUS
examination was 4 months and the
oldest patient with a patent metopic
suture was 9 months of age.
The limitation of our study is the
moderate sample size resulted
in a relatively small number of
closed sutures, which limits the
value of assessments of interreader
disagreement, because a single
disagreement can lead to a greatly
reduced κ. However, the patient
population was accumulated over
a period of 2.5 years in a tertiary
care children’s hospital and this
is the largest series evaluating the
performance of CUS for detection of
craniosynostosis in children, referred
for imaging study by pediatricians
and family practitioners.
CONCLUSIONS
The current series suggests that
cranial ultrasound, a radiation-free
technique, could be used as the
first-line imaging tool for exclusion
or detection of craniosynostosis in
children up to 12 months, reducing
the need of initial radiographs in
young children. Metopic suture
evaluation remains challenging
for both CUS and radiography,
and additional assessment may be
required. These findings warrant
assessment and replication in larger
prospective studies.
ACKNOWLEDGMENTS
We thank Joanne Zabihaylo for
administrative support, Shifra
Fraifeld for editorial work, and
Yael Kamil (Clinical Research Unit,
Children’s Hospital of Eastern
Ontario) for REDCap System support.
We thank our sonographers for the
collaboration with the ultrasound
studies. We are grateful to the
families who consented to take part
in the study, and to the medical
imaging staff members of the
Children’s Hospital of Ottawa, who
participated in caring for the infants.
8
Address correspondence to Katya Rozovsky, MD, Department of Diagnostic Imaging, HSC, CS-121, Children's Hospital of Winnipeg, University of Manitoba, GA216-
820 Sherbrook Street, Winnipeg, MB R3T 2N2 Canada. E-mail: [email protected]
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2016 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no fi nancial relationships relevant to this article to disclose.
FUNDING: The authors thank the Provincial Academic Health Science Center Alternative Funding Plan Innovation Fund of the Ontario Medical Association, and the
Ministry of Health and Long-Term Care for fi nancial support.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential confl icts of interest to disclose.
ABBREVIATIONS
CT: computed tomography
CUS: cranial ultrasound
REDCap: Research Electronic
Data Capture
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
PEDIATRICS Volume 137 , number 2 , February 2016
REFERENCES
1. Boulet SL, Rasmussen SA, Honein
MA. A population-based study of
craniosynostosis in metropolitan
Atlanta, 1989-2003.Am J Med Genet A.
2008;146A(8):984–991
2. Kotrikova B, Krempien R,
Freier K, Mühling J. Diagnostic
imaging in the management of
craniosynostoses.Eur Radiol.
2007;17(8):1968–1978
3. Stenirri S, Restagno G, Ferrero GB, et
al. Integrated strategy for fast and
automated molecular characterization
of genes involved in craniosynostosis.
Clin Chem. 2007;53(10):1767–1774
4. Bellew M, Chumas P, Mueller R,
Liddington M, Russell J. Pre- and
postoperative developmental
attainment in sagittal synostosis.
Arch Dis Child. 2005;90(4):
346–350
5. Kapp-Simon KA, Speltz ML,
Cunningham ML, Patel PK, Tomita
T. Neurodevelopment of children
with single suture craniosynostosis:
a review.Childs Nerv Syst.
2007;23(3):269–281
6. Shipster C, Hearst D, Somerville A,
Stackhouse J, Hayward R, Wade A.
Speech, language, and cognitive
development in children with isolated
sagittal synostosis.Dev Med Child
Neurol. 2003;45(1):34–43
7. Speltz ML, Collett BR, Wallace ER, et al.
Intellectual and academic functioning of
school-age children with single-suture
craniosynostosis.Pediatrics. 2015;135(3).
Available at: www. pediatrics. org/ cgi/
content/ full/ 135/ 3/ e615
8. Tamburrini G, Caldarelli M, Massimi
L, Santini P, Di Rocco C. Intracranial
pressure monitoring in children
with single suture and complex
craniosynostosis: a review.Childs Nerv
Syst. 2005;21(10):913–921
9. Badve CA, K MM, Iyer RS, Ishak
GE, Khanna PC. Craniosynostosis:
imaging review and primer on
computed tomography.Pediatr Radiol.
2013;43(6):728–742, quiz 725–727
10. Frassanito P, Di Rocco C. Depicting
cranial sutures: a travel into
the history.Childs Nerv Syst.
2011;27(8):1181–1183
11. Gellad FE, Haney PJ, Sun JC, Robinson
WL, Rao KC, Johnston GS. Imaging
modalities of craniosynostosis with
surgical and pathological correlation.
Pediatr Radiol. 1985;15(5):285–290
12. Nagaraja S, Anslow P, Winter B.
Craniosynostosis.Clin Radiol.
2013;68(3):284–292
13. Richtsmeier JT, Grausz HM, Morris GR,
Marsh JL, Vannier MW. Growth of the
cranial base in craniosynostosis.Cleft
Palate Craniofac J. 1991;28(1):55–67
14. Branson HM, Shroff MM.
Craniosynostosis and 3-dimensional
computed tomography.Semin
Ultrasound CT MR. 2011;32(6):
569–577
15. Alizadeh H, Najmi N, Mehdizade M,
Najmi N. Diagnostic accuracy of
ultrasonic examination in suspected
craniosynostosis among infants.Indian
Pediatr. 2013;50(1):148–150
16. Regelsberger J, Delling G, Helmke K,
et al. Ultrasound in the diagnosis of
craniosynostosis.J Craniofac Surg.
2006;17(4):623–625, discussion
626–628
17. Regelsberger J, Delling G, Tsokos
M, et al. High-frequency ultrasound
confi rmation of positional
plagiocephaly.J Neurosurg.
2006;105(suppl 5):413–417
18. Saponaro G, Bernardo S, Di Curzio P,
et al. Cranial sutures ultrasonography
as a valid diagnostic tool in isolated
craniosynostoses: a pilot study.Eur J
Plast Surg. 2014;37(2):77–84
19. Simanovsky N, Hiller N, Koplewitz
B, Rozovsky K. Effectiveness of
ultrasonographic evaluation of the
cranial sutures in children with
suspected craniosynostosis.Eur Radiol.
2009;19(3):687–692
20. Soboleski D, McCloskey D, Mussari
B, Sauerbrei E, Clarke M, Fletcher
A. Sonography of normal cranial
sutures.AJR Am J Roentgenol.
1997;168(3):819–821
21. Soboleski D, Mussari B, McCloskey
D, Sauerbrei E, Espinosa F, Fletcher
A. High-resolution sonography of
the abnormal cranial suture.Pediatr
Radiol. 1998;28(2):79–82
22. Linz C, Collmann H, Meyer-Marcotty
P, et al. Occipital plagiocephaly:
unilateral lambdoid synostosis versus
positional plagiocephaly.Arch Dis Child.
2015;100(2):152–157
23. Krimmel M, Will B, Wolff M, et al.
Value of high-resolution ultrasound
in the differential diagnosis of
scaphocephaly and occipital
plagiocephaly.Int J Oral Maxillofac
Surg. 2012;41(7):797–800
24. Sze RW, Parisi MT, Sidhu M, et al.
Ultrasound screening of the lambdoid
suture in the child with posterior
plagiocephaly.Pediatr Radiol.
2003;33(9):630–636
25. Ngo AV, Sze RW, Parisi MT, et al. Cranial
suture simulator for ultrasound
diagnosis of craniosynostosis.Pediatr
Radiol. 2004;34(7):535–540
26. Brenner D, Elliston C, Hall E, Berdon
W. Estimated risks of radiation-
induced fatal cancer from
pediatric CT.AJR Am J Roentgenol.
2001;176(2):289–296
27. Kleinerman RA. Cancer risks following
diagnostic and therapeutic radiation
exposure in children.Pediatr Radiol.
2006;36(suppl 2):121–125
28. Schweitzer T, Böhm H, Meyer-Marcotty
P, Collmann H, Ernestus RI, Krauß J.
Avoiding CT scans in children with
single-suture craniosynostosis.Childs
Nerv Syst. 2012;28(7):1077–1082
29. Bredero-Boelhouwer H, Treharne
LJ, Mathijssen IM. A triage system
for referrals of pediatric skull
deformities.J Craniofac Surg.
2009;20(1):242–245
30. Weinzweig J, Kirschner RE, Farley A,
et al. Metopic synostosis: defi ning the
temporal sequence of normal suture
fusion and differentiating it from
synostosis on the basis of computed
tomography images.Plast Reconstr
Surg. 2003;112(5):1211–1218
31. Vu HL, Panchal J, Parker EE, Levine NS,
Francel P. The timing of physiologic
closure of the metopic suture: a review
of 159 patients using reconstructed 3D
CT scans of the craniofacial region.J
Craniofac Surg. 2001;12(6):527–532
9 by guest on April 3, 2020www.aappublications.org/newsDownloaded from
originally published online January 15, 2016; Pediatrics Simanovsky and Elka Miller
Katya Rozovsky, Kristin Udjus, Nagwa Wilson, Nicholas James Barrowman, NataliaCranial Ultrasound as a First-Line Imaging Examination for Craniosynostosis
ServicesUpdated Information &
015-2230http://pediatrics.aappublications.org/content/early/2016/01/14/peds.2including high resolution figures, can be found at:
References
015-2230#BIBLhttp://pediatrics.aappublications.org/content/early/2016/01/14/peds.2This article cites 31 articles, 4 of which you can access for free at:
Subspecialty Collections
http://www.aappublications.org/cgi/collection/radiology_subRadiologyhttp://www.aappublications.org/cgi/collection/safety_subSafety_management_subhttp://www.aappublications.org/cgi/collection/administration:practiceAdministration/Practice Managementfollowing collection(s): This article, along with others on similar topics, appears in the
Permissions & Licensing
http://www.aappublications.org/site/misc/Permissions.xhtmlin its entirety can be found online at: Information about reproducing this article in parts (figures, tables) or
Reprintshttp://www.aappublications.org/site/misc/reprints.xhtmlInformation about ordering reprints can be found online:
by guest on April 3, 2020www.aappublications.org/newsDownloaded from
originally published online January 15, 2016; Pediatrics Simanovsky and Elka Miller
Katya Rozovsky, Kristin Udjus, Nagwa Wilson, Nicholas James Barrowman, NataliaCranial Ultrasound as a First-Line Imaging Examination for Craniosynostosis
http://pediatrics.aappublications.org/content/early/2016/01/14/peds.2015-2230located on the World Wide Web at:
The online version of this article, along with updated information and services, is
1073-0397. ISSN:60007. Copyright © 2016 by the American Academy of Pediatrics. All rights reserved. Print
the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois,has been published continuously since 1948. Pediatrics is owned, published, and trademarked by Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
by guest on April 3, 2020www.aappublications.org/newsDownloaded from