Cranial Ultrasound as a First- Line Imaging Examination ......for evaluation of the cranial sutures...

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ARTICLE PEDIATRICS Volume 137, number 2, February 2016:e20152230 Cranial Ultrasound as a First- Line Imaging Examination for Craniosynostosis Katya Rozovsky, MD, a,b Kristin Udjus, MD, a Nagwa Wilson, MD, PhD, a Nicholas James Barrowman, PhD, c Natalia Simanovsky, MD, b Elka Miller, MD a abstract BACKGROUND: 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. a Department of Medical Imaging, and c Research Institute, Children’s Hospital of Eastern Ontario, University of Ottawa, Ottawa, Ontario, Canada; and b Department 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 final 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 first-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 first-line imaging study for diagnosis or exclusion of craniosynostosis, reducing exposure to ionizing radiation in this vulnerable population. by guest on April 3, 2020 www.aappublications.org/news Downloaded from

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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.

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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.

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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.

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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.

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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).

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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.

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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.

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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

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PEDIATRICS Volume 137 , number 2 , February 2016

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