Gerda Meijler

Sylke J. Steggerda

Neonatal Cranial
Ultrasonography
Third Edition

123
Neonatal Cranial Ultrasonography
Gerda Meijler • Sylke J. Steggerda

Neonatal Cranial
Ultrasonography
Third Edition
Gerda Meijler Sylke J. Steggerda
Department of Neonatology Department of Neonatology
Isala Women and Children’s Hospital Leiden University Medical Center
Zwolle Leiden
The Netherlands The Netherlands

Illustrated by
Amanda Gautier
Gautier Scientific Illustration
Groningen
The Netherlands

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 Foreword

This is now the third edition of Neonatal Cranial Ultrasonography by Gerda

Meijler and Sylke J. Steggerda, both well-known experts in the field of
neuro-imaging in the newborn. The ultrasound images have improved even
further in this edition with the use of better equipment showing the even
more detailed information that can now be obtained using this non-invasive
bedside technique. The book is very well illustrated and there are videos
available online, showing those who are just starting to learn the technique
how to place the probe for different acoustic windows, adjust the machine
and what to look for. The size of the book makes it easy to have to hand for
comparing images made by the trainee and those shown in the atlas.
Not only is normal anatomy very well shown, there is a chapter illustrat-
ing the progress in brain maturation from extremely preterm to term infants
that can be visualised using cranial ultrasound. Scoring systems one can use
for intraventricular and cerebellar haemorrhages and white matter injury
are well described. There are some correlates with MRI of the brain which
are also helpful and illustrate how much can be seen with both techniques.
Calcification, for example lenticulostriate vasculopathy, will not be visible
on conventional MRI techniques, small cysts are difficult to see on MRI
and myelination cannot be seen on ultrasound, showing that these two tech-
niques are complementary. Doppler ultrasonography is well explained and
illustrated.
There is not enough space for all the different pathologies one may
encounter in a newborn infant (metabolic disorders; neurocutaneous phaco-
matoses) but with the help of many references, one will find a relevant
recent publication or book.

v
vi Foreword

This pocket-sized book can and should be carried by every trainee who
is learning how to perform cranial ultrasound, and he or she is likely to
become as enthusiastic as these two authors have been for many years.

Frances M. Cowan
Imperial College London
London, UK
University of Bristol
Bristol, UK

Linda S. de Vries
Neonatal Neurology
University Medical Center
Utrecht, The Netherlands
 Acknowledgements

We want to thank the children whose photographs and videos have been
used for this book and their parents for their permission to use the photo-
graphs and videos.
We also want to thank Professor Frances Cowan for reviewing Chap. 9
and for her useful and thorough comments, and Professor Linda de Vries
for her general advice and comments, and for providing some figures.
We thank Gerrit Kracht, medical photographer, for making the colour
videos.

vii
 Contents

Part I The Cranial Ultrasound Procedure

1 Neonatal Cranial Ultrasonography:
Advantages and Aims�������������������������������������������������������������  3
1.1 Introduction���������������������������������������������������������������������  3
1.2 Advantages of Cranial Ultrasonography�������������������������  3
1.3 Aims of Neonatal Cranial Ultrasonography �������������������  4
Further Reading �����������������������������������������������������������������������  5
2 Cranial Ultrasonography: Technical Aspects�����������������������  7
2.1 Equipment �����������������������������������������������������������������������  7
2.1.1 Ultrasound Machine���������������������������������������������  7
2.1.2 Transducers ���������������������������������������������������������  7
2.2 Data Management ����������������������������������������������������������� 20
2.3 Safety������������������������������������������������������������������������������� 20
Further Reading ����������������������������������������������������������������������� 21
3 Performing Cranial Ultrasound Examinations ������������������� 23
3.1 Settings����������������������������������������������������������������������������� 23
3.1.1 Scan Depth����������������������������������������������������������� 23
3.1.2 Scan Area������������������������������������������������������������� 26
3.1.3 Gain��������������������������������������������������������������������� 29
3.1.4 Transducer Frequency����������������������������������������� 31
3.1.5 Focus Point����������������������������������������������������������� 32
3.2 Anterior Fontanelle Views����������������������������������������������� 35
3.2.1 Coronal Planes����������������������������������������������������� 36
3.2.2 Sagittal Planes����������������������������������������������������� 36
3.3 Supplemental Acoustic Windows������������������������������������� 39
3.3.1 Posterior Fontanelle��������������������������������������������� 41

ix
x Contents

3.3.2 Temporal Windows ��������������������������������������������� 48

3.3.3 Mastoid Fontanelles��������������������������������������������� 51
Appendix: Indications for Scanning Through
Supplemental Windows������������������������������������������������������������� 57
Further Reading ����������������������������������������������������������������������� 58
4  ssessing Cranial Ultrasound Examinations�����������������������
A 59
4.1 Assessing Cranial Ultrasound Examinations������������������� 59
4.1.1 A Systematic Approach for Detecting Cerebral
Pathology������������������������������������������������������������� 59
Appendix: Measurement of the Lateral Ventricles������������������� 83
References��������������������������������������������������������������������������������� 83
Further Reading ����������������������������������������������������������������������� 84
5 Timing of Ultrasound Examinations������������������������������������� 85
5.1 Timing of Ultrasound Examinations������������������������������� 85
5.1.1 Ultrasound Screening������������������������������������������� 85
5.1.2 Cranial Ultrasonography
at Term-Corrected Age�����������������������������������������128
Appendix 5.1: Recommendations for
CUS Examinations����������������������������������������������������������������� 132
Appendix 5.2: How to Distinguish Physiological from
Pathological Echodensities in the White Matter��������������������� 135
References���������������������������������������������������������������������������������136
Further Reading ��������������������������������������������������������������������� 136
6 Scoring Systems�����������������������������������������������������������������������139
6.1 Scoring Systems���������������������������������������������������������������139
Appendix 6.1: Classification of GMH-IVH��������������������������� 139
Appendix 6.2: Classification of CBH������������������������������������� 153
Appendix 6.3: Classification of PVE ������������������������������������� 164
Appendix 6.4: Classification of PVL ������������������������������������� 169
References���������������������������������������������������������������������������������181
Further Reading ��������������������������������������������������������������������� 182
Contents xi

7 Limitations of Cranial Ultrasonography and

Recommendations for MRI���������������������������������������������������183
7.1 Limitations of Cranial Ultrasonography �������������������������183
7.2 Role of MRI���������������������������������������������������������������������184
7.2.1 Conditions in Which MRI Contributes
to Diagnosis and/or prognostication �������������������191
7.3 Role of CT�����������������������������������������������������������������������192
Appendix: Indications for Neonatal MRI Examinations ���������192
References���������������������������������������������������������������������������������193
Further Reading �����������������������������������������������������������������������193
8 Maturational Changes of the Neonatal Brain ���������������������195
8.1 Maturational Processes ���������������������������������������������������195
8.2 Gyration���������������������������������������������������������������������������195
8.3 Germinal Matrix �������������������������������������������������������������196
8.4 Cell Migration�����������������������������������������������������������������210
8.5 Deep Grey Matter Changes���������������������������������������������211
8.6 Changes in Cerebrospinal Fluid Spaces���������������������������213
Further Reading �����������������������������������������������������������������������216
9 Transcranial Doppler Sonography in Neonates�������������������219
9.1 Machine Settings�������������������������������������������������������������219
9.2 Performing Doppler Examination�����������������������������������223
9.2.1 Imaging Cerebrovascular Anatomy���������������������223
9.2.2 Assessing Cerebral Blood Flow Patterns and
Velocities�������������������������������������������������������������236
9.3 Clinical Application of Doppler Assessment�������������������242
9.3.1 Clinical Importance of Assessing
Cerebral Blood Flow Velocity�����������������������������242
9.3.2 Clinical Importance of Assessing
Cerebrovascular Anatomy�����������������������������������250
References���������������������������������������������������������������������������������256
xii Contents

Part II Ultrasound Anatomy of the Neonatal Brain

10 Coronal Planes Anterior Fontanelle�������������������������������������263
11 Sagittal Planes Anterior Fontanelle���������������������������������������285
12 Posterior Fontanelle ���������������������������������������������������������������303
13 Temporal Window�������������������������������������������������������������������315
14 Mastoid Fontanelle�����������������������������������������������������������������321
 Abbreviations

ACA Anterior cerebral artery

aCM Callosal marginal artery
aFI Frontal internal arteries
AHW Anterior horn width
aPC Pericallosal artery
CBH Cerebellar haemorrhage(s)
CDI Colour Doppler imaging
CNS Central nervous system
c-PVL Cystic periventricular leukomalacia
CUS Cranial ultrasound/ultrasonography
CV Convex
ECMO Extracorporeal membrane oxygenation
GA Gestational age
GMH Germinal matrix haemorrhage
GMH-IVH Germinal matrix-intraventricular haemorrhage
ICA Internal carotid artery
ICV Internal cerebral vein
ISS Inferior sagittal sinus
IVH Intraventricular haemorrhage
LA Linear array
LSV Lenticulostriate vasculopathy
MCA Middle cerebral artery
MRI Magnetic resonance imaging
NICU Neonatal intensive care unit
PA Phased array
PCA Posterior cerebral artery
PHVD Post-haemorrhagic ventricular dilatation

xiii
xiv Abbreviations

PVE Periventricular echodensities or periventricular echogenicity

PVHI Periventricular haemorrhagic infarction
PVL Periventricular leukomalacia
PW Pulsed wave
PWML Punctate white matter lesions
RI Resistance index
SCA Superior cerebellar artery
SSS Superior sagittal sinus
ST Transverse sinus
TEA Term equivalent age
TOD Thalamo-occipital distance
TRV Transverse sinus(es)
TV Terminal veins
VI Ventricular index
VOG Vein of Galen
PART I THE CRANIAL ULTRASOUND
PROCEDURE
 1 Neonatal Cranial Ultrasonography:
Advantages and Aims

1.1 I ntroduction

Cranial ultrasonography (CUS) is the preferred modality for visualising the

brain of the sick and/or preterm neonate. It uses the unique features of the
neonatal skull with its open fontanelles and sutures to look into the brain
and has important advantages above other imaging modalities.

1.2 A
 dvantages of Cranial Ultrasonography

Major advantages of CUS are:

• It can be performed at the bedside, on the lap or in the cot with little
disturbance to the neonate (Fig. 1.1; see also Chap. 3).
• It can be performed immediately after birth and repeated as often as nec-
essary. It thereby enables visualisation of ongoing brain growth and mat-
uration and the changes of brain lesions over time. In addition, it can be
used to assess the timing of brain injury.
• It is safe.
• It is a reliable tool for the detection of most haemorrhagic brain lesions
in preterm and full-term neonates.
• It is a helpful tool for the detection of ischaemic brain lesions as well as
cerebral infections, and major structural brain anomalies, in both pre-
term and full-term neonates.
• Some abnormalities (including lenticulostriate vasculopathy [LSV], cal-
cifications and germinolytic cysts) are only or better detected by CUS as
compared to other neuro-imaging modalities.
© Springer Nature Switzerland AG 2019 3
G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
4 1 Neonatal Cranial Ultrasonography: Advantages and Aims

Fig. 1.1 Cranial ultrasound procedure performed in a neonate in its cot

• Doppler flow velocity measurements of the cerebral vessels can be per-

formed during the same examination.
• It is relatively inexpensive as compared to other neuroimaging tech-
niques and therefore also a very feasible neuroimaging modality in low-­
income countries.

For all these reasons, CUS is an excellent tool for serial brain imaging
during the neonatal period and thereafter until closure of the fontanelles.

1.3 A
 ims of Neonatal Cranial Ultrasonography

The aims of neonatal CUS are to assess:

• Brain growth and maturation
• The presence of structural brain abnormalities and/or brain injury
• The timing of injury
Further Reading 5

CUS also helps in determining the neurological prognosis of the

neonate.
In sick neonates and in neonates with serious brain abnormalities, either
congenital or acquired, it plays an important role in decision making
regarding the continuation or redirection of intensive care. In neonates with
brain injury, it may help to optimise treatment and support of the neonate
and its family, both during the neonatal period and thereafter.

Advantages of CUS Aims of CUS

Safe Follow brain growth and maturation
Exclude/demonstrate brain pathology
Bedside-compatible Follow lesions over time
Assess timing of injury
Enables early imaging Estimate neurological prognosis
Enables serial imaging Optimise treatment and support
–– Brain maturation
–– Brain growth
–– Evolution of lesions
Inexpensive
Suitable for screening

Further Reading

Bracci R et al (2006) The timing of neonatal brain damage. Biol Neonate 90:145–155
Daneman A, Epelman M (2015) Neurosonography: in pursuit of an optimised examina-
tion. Pediatr Radiol 45:S406–S412
Epelman M et al (2012) Ultrasound and MR imaging in the evaluation of neonatal enceph-
alopathy: competitive or complementary imaging studies? Magn Reson Imaging Clin
N Am 20:93–115
Govaert P, De Vries LS (2010) An atlas of neonatal brain sonography, 2nd edn. MacKeith
Press, Cambridge
Hagmann CF et al (2010) Cranial ultrasound findings in well Ugandan infants. Arch Dis
Child Fetal Neonatal Ed 95:F338–F344
Leijser LM et al (2006) Using cerebral ultrasound effectively in the newborn infant. Early
Hum Dev 82:827–835
6 1 Neonatal Cranial Ultrasonography: Advantages and Aims

Mazmanyan PA et al (2016) Preterm cranial ultrasound scanning is both feasible and

effective in a middle-income country. Acta Paediatrica 105:291–299
Meijler et al (2016) Neonatal cranial ultrasonography. Diagnostic pediatric ultrasound,
1st edn. Beek and van Rijn
Neil, Volpe (2017) Specialized neurological studies. In: Volpe’s neurology of the newborn,
6th edn. Elsevier
Plaisier A et al (2015) Serial cranial ultrasonography or early MRI for detecting preterm
brain injury? Arch Dis Child Fetal Neonatal Ed 100:F293–F300
Sisman J et al (2018) Lenticluostriate vasculopathy in preterm infants: a new classification,
clinical association and neurodevelopmental outcome. J Perinatol 38:1370–1378
Skiöld B et al (2019) A novel scoring system for term-equivalent-age cranial ultrasound in
extremely preterm infants. Ultrasound Med Biol 45:786–794
Steggerda SJ et al (2009) Neonatal cranial ultrasonography: how to optimise its perfor-
mance. Early Hum Dev 85:93–99
Tann CJ et al (2016) Early cranial ultrasound findings among infants with neonatal
encephalopathy in Uganda: an observational study. Pediatr Res 80:190–196
The British Medical Ultrasound Society (BMUS) (2009) Guidelines for the safe use of
diagnostic ultrasound equipment. [Link]/static/uploads/resources/BMUS-
[Link]
de Vries LS et al (2004) Ultrasound abnormalities preceding cerebral palsy in high-risk
preterm infants. J Pediatr 144:815–820
de Vries LS et al (2006) The role of cranial ultrasound and magnetic resonance imaging in
the diagnosis of infections of the central nervous system. Early Hum Dev 82:819–825
de Vries, Volpe (2017) Viral, protozoan and related intracranial infections. In: Volpe’s neu-
rology of the newborn, 6th edn. Elsevier
de Vries, Volpe (2017) Bacterial and fungal intracranial infections. In: Volpe’s neurology
of the newborn, 6th edn. Elsevier
Verboon-Maciolek MA et al (2006) White matter damage in neonatal enterovirus menin-
goencephalitis. Neurology 66:1267–1269
Verboon-Maciolek MA et al (2008) Human parechovirus causes encephalitis with white
matter injury in neonates. Ann Neurol 64:266–273
Vollmer B et al (2003) Predictors of long-term outcome in very preterm infants: gesta-
tional age versus neonatal cranial ultrasound. Pediatrics 112:1108–1114
van Wezel-Meijler G et al (2010) Cranial ultrasonography in neonates: role and limita-
tions. Semin Perinatol 34:28–38
van Wezel-Meijler G et al (2011) Ultrasound detection of white matter injury in very pre-
term neonates: practical implications. Dev Med Child Neurol 53(Suppl 4):29–34
van Wezel-Meijler GV, De Vries LS (2014) Cranial ultrasound—optimising utility in the
NICU. Curr Pediatr Rev 10(1):16–27
Yikilmaz A, Taylor GA (2008) Cranial sonography in term and near-term infants. Pediatr
Radiol 38:606–616
 2 Cranial Ultrasonography:
Technical Aspects

For good-quality and safe CUS examinations, the following conditions need
to be fulfilled: a high-quality modern ultrasound machine with appropriate
transducers to enable optimal image quality and a sonographer who is
aware of the special needs of the sick and/or preterm neonate and who is
sufficiently experienced in CUS.

2.1 E
 quipment

2.1.1 U
 ltrasound Machine

The ultrasound machine should be a transportable real-time scanner, allowing

bedside examinations without the need to transport the baby (see Fig. 1.1). It
should be equipped with transducers that are appropriate for CUS, adapted
software for CUS and Doppler assessments (see Chap. 9) and a reliable digital
storage system. Settings need to be optimised for neonatal brain imaging. It is
recommended that preprogrammed presets be used for CUS imaging in both
preterm and full-term neonates. These settings can be further optimised in
individual cases and under certain circumstances (see Chap. 3).

2.1.2 T
 ransducers

The use of a convex (CV) or curved array transducer is recommended. The

transducer should be appropriately sized for an almost perfect fit on the
anterior fontanelle (Fig. 2.1). To allow good contact between the transducer
and the skin, ultrasound gel is used. We preferably use a micro CV
­transducer (see Fig. 2.1). If the fontanelle is very small, or when hats are
© Springer Nature Switzerland AG 2019 7
G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
8 2 Cranial Ultrasonography: Technical Aspects

used for fixation of ventilatory support systems, a smaller phased array (PA)
probe can be used, but the field of view is smaller and the image quality less
than that of the CV probe (Fig. 2.2).

Fig. 2.1 (a) Well-fitting CV probe, positioned on the anterior fontanelle. (b) Coronal
CUS scan at the level of the bodies of the lateral ventricles performed with micro CV
probe in extremely preterm infant gestational age (GA) 25 weeks, scanned on the sec-
ond day after birth. The whole brain is well depicted
2.1 Equipment 9

Fig. 2.2 (a) Smaller PA probe, positioned on the anterior fontanelle. (b) Coronal CUS
scan in very preterm neonate performed with PA probe. Due to the small scan area, the
periventricular white matter cannot be well assessed (compare with Fig. 2.1b). (c, d)
Coronal CUS scans at the level of the bodies of the lateral ventricles in a preterm neo-
nate with posthaemorrhagic ventricular dilatation (PHVD). (c) Performed with a PA
probe: the wide ventricles are filling the image and hamper visualization of the peri-
ventricular white matter (arrow). (d) Performed with a CV probe: thanks to the larger
scan area, the periventricular white matter (arrow) is now well depicted
10 2 Cranial Ultrasonography: Technical Aspects

Fig. 2.2 (continued)

2.1 Equipment 11

Thanks to the high scan frequency and the parallel ultrasound beam,
linear array (LA) probes provide superb near-field resolution. Because of
their large footprint (Fig. 2.3) and suboptimal far-field resolution, they are
not suitable for routine CUS examinations. However, they provide detailed

Fig. 2.3 (a) LA probe, positioned on the anterior fontanelle. (b, c) Coronal CUS in a very
preterm neonate at the level of bodies of the lateral ventricles, using the CV probe and
transducer frequency of 10 MHz (b) and LA probe with transducer frequency set at
18 MHz (c), showing the superb near-field resolution of the LA probe. However, the
overall view of the brain is less well defined using the LA probe
12 2 Cranial Ultrasonography: Technical Aspects

Fig. 2.3 (continued)

views of superficial structures (cortex, subcortical white matter, subarach-

noidal and subdural spaces) and can demonstrate flow in the superior sagit-
tal sinus (see Chap. 9) (Fig. 2.4).
The higher the transducer frequency, the better the near-field resolution.
A lower transducer frequency will provide a lower resolution, but a better
penetration (see Chap. 3). The ultrasound system should therefore be
equipped with multifrequency transducers (5–7.5(8)–10 (11) MHz).
Neonates have relatively small heads. Therefore, high-­quality images can
usually be obtained with the transducer frequency set at 7.5–8 MHz. In
most neonates this enables good visualisation of the whole brain. For better
evaluation of the most superficial structures and/or in very tiny infants with
tiny heads, we advise performing additional scanning, using a higher fre-
quency up to 10 or 11 MHz, thus obtaining a higher near-­field resolution
(Fig. 2.5). If, on the other hand, deeper penetration of the beam is required,
as in larger, older infants or infants with thick, curly hair or to obtain a bet-
ter view of the deeper structures, additional scanning with a lower fre-
quency (around 5 MHz) is recommended (Fig. 2.6).
2.1 Equipment 13

Fig. 2.4 (a–d) CUS in full-term neonate with GBS sepsis/meningitis. (a) (coronal) and
(b) (parasagittal) scans performed with CV probe, (c) (coronal) and (d) (parasagittal)
scans performed with LA probe. With the CV probe, a good overview of the brain is
obtained, showing increased echogenicity around the cortex (arrows), indicating cor-
tical injury, and in the ventricular wall (green arrows), suggesting ventriculitis. The
images performed with the LA probe are of superb resolution and show more detail of
the cortical injury (arrows), but the overview of the brain is lost. (e–g) CUS scans per-
formed in a full-term baby with intractable seizures. (e) Parasagittal scan performed
with a CV probe. (f) Parasagittal scan performed with a LA probe, showing the swollen
cortex (arrows) in more detail.
14 2 Cranial Ultrasonography: Technical Aspects

Fig. 2.4 (continued) (g) Colour Doppler scan using the LA probe, demonstrating flow
in superficial cortical arteries and the superior sagittal sinus (green arrow). (h, i) CUS in
a very preterm neonate. (h) Parasagittal scan through the insular area performed with
the CV probe shows inhomogeneous echogenicity of the white matter (arrow). (i) The
LA probe shows that the echogenicity extends deeper into the white matter (arrow).
However, the overall view of the brain is lost
2.1 Equipment 15

Fig. 2.4 (continued)

16 2 Cranial Ultrasonography: Technical Aspects

Fig. 2.4 (continued)

2.1 Equipment 17

Fig. 2.4 (continued)

Fig. 2.5 Same full-term baby with intractable seizures as Fig. 2.4e–g. (a) Parasagittal
scan performed with scan frequency set at 8 MHz. (b) scan frequency set at 10 MHz. In
(b) the resolution is better, and the superficial structures (cortex (arrow)) and subcorti-
cal white matter (green arrow) are depicted in more detail
18 2 Cranial Ultrasonography: Technical Aspects

Fig. 2.5 (continued)

Fig. 2.6 (a, b) Coronal CUS scans in a full-term neonate, scanned with a transducer
frequency of, respectively, 8 (a) and 5 (b) MHz. A good resolution is obtained with the
high scan frequency, while with the lower frequency, the resolution is less, but the
cerebellum (arrow) is somewhat better depicted.
2.1 Equipment 19

Fig. 2.6 (continued) (c, d) Coronal CUS scans in ex-preterm baby scanned at a cor-
rected age of 6 months (mild ventriculomegaly due to an intraventricular haemor-
rhage in the neonatal period). (c) Scan frequency set at 8 MHz, showing poor
penetration due to the large size of the head and therefore large distance between the
transducer and the brain structures. (d) Scan frequency set at 5 MHz, showing better
penetration into the brain
20 2 Cranial Ultrasonography: Technical Aspects

Fig. 2.6 (continued)

2.2 D
 ata Management

Images need to be reviewable. Therefore, it is recommended that a dedi-

cated digital storage system be used, allowing reliable storage and post-­
imaging assessment and measurements. Relevant patient information
(name, date of birth, date of examination and hospital number) should be
adequately stored with the ultrasound images.

2.3 S
 afety

The sonographer or the physician should be trained to perform safe, reliable

CUS examinations. In addition, he or she should be well informed with regard
to the normal anatomy and specific features of the neonatal brain and to the
­maturational phenomena occurring in the (preterm) neonate’s brain. He or
she also needs to be well informed about frequently occurring, often age-­
specific brain anomalies whether congenital or acquired and be able to recog-
nise these and look for them. The sonographer should also be aware of the
special needs of vulnerable, sick (preterm) neonates and should take the nec-
Further Reading 21

essary hygiene precautions. This includes appropriate clothing, hand hygiene

and cleaning of the ultrasound machine and transducers according to hospi-
tal regulations. The ultrasound gel is preferably sterile and stored at room
temperature. Cooling of the infant due to opening of the incubator needs to
be avoided.

CUS equipment and

procedure Transducers
• Modern, transportable • Multifrequency 5–11 MHz
ultrasound machine – Preferably CV probe
• Special CUS software • Appropriately sized
• Standard CUS settings; • Standard examination: 7.5 or 8 MHz
adjust when needed • Tiny infant and/or superficial
• Digital storage system structures: use additional higher
• Avoid manipulation and frequency (10 or 11 MHz)
cooling of infant • Large infant, thick hair, and/or deep
• Take necessary (hygiene) structures: use additional lower
precautions frequency (4–6 MHz)

Further Reading

Couture A et al (2001) Advanced cranial ultrasound: transfontanellar Doppler imaging in

neonates. Eur Radiol 11:2399–2341
Daneman A, Epelman M (2015) Neurosonography: in pursuit of an optimised examina-
tion. Pediatr Radiol 45:S406–S412
Ecury-Goossen GM et al (2015) State of the art cranial ultrasound imaging in neonates.
J Vis Exp 2:e52238
Miller E et al (2012) Colour Doppler US of normal cerebral venous sinuses in neonates: a
comparison with MR venography. Pediatr Radiol 42:1070–1079
Meijler G et al (2016) Neonatal cranial ultrasonography. Diagnostic pediatric ultrasound,
1st edn. Beek E, van Rijn RR
Steggerda SJ et al (2009) Neonatal cranial ultrasonography: how to optimise its perfor-
mance. Early Hum Dev 85:93–99
van Wezel-Meijler G et al (2010) Cranial ultrasonography in neonates: role and limita-
tions. Semin Perinatol 34:28–38
van Wezel-Meijler G, de Vries LS (2014) Cranial ultrasound—optimising utility in the
NICU. Curr Pediatr Rev 10(1):16–27
 3 Performing Cranial Ultrasound
Examinations

Preterm infants and sick full-term infants are examined in their incubator
while maintaining monitoring of vital functions (see also Chap. 2 and
Fig. 1.1). It is recommended that the CUS examination is performed with
only the incubator windows open to avoid temperature loss. Manipulation
of the infant (with the exception of minor adjustments) is rarely necessary
while scanning through the anterior fontanelle. Older infants and full-term,
well neonates can be examined in their cot or car seat or on an adult’s lap
(Fig. 3.1).
Make sure that the ultrasound transducer and cables have been cleaned
prior to each examination (this should be done with a special cleanser, suit-
able for cleaning ultrasound equipment), and apply enough gel to provide
good contact between the transducer and the skin. Consider using sterile
and/or warmed ultrasound gel, especially for extremely premature infants
(Fig. 3.2).

3.1 S
 ettings

It is recommended to use standard CUS presets. These can be applied for

most routine CUS examinations and adapted when needed.

3.1.1 S
 can Depth

When starting the CUS examination, depending on the size of the head, adap-
tation of the depth of the scan window may be necessary to obtain an image
that fills the sector window and shows the whole depth of the brain (Fig. 3.3).

© Springer Nature Switzerland AG 2019 23

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
24 3 Performing Cranial Ultrasound Examinations

Fig. 3.1 Ultrasound examination performed around term-equivalent age (TEA) in two
ex-preterm infants in an outpatient setting: (a) while the infant is on her mother’s lap
and (b) while the infant is in its stroller
3.1 Settings 25

Fig. 3.2 (a) Cleaning of ultrasound transducer. (b) Application of sterile ultrasound gel
26 3 Performing Cranial Ultrasound Examinations

Fig. 3.3 Coronal ultrasound scan in a preterm infant with adaptation of depth. (a) Scan
window too small, posterior fossa is not seen. This is a common flaw. (b) Appropriate
depth, CUS image fits within scan window. (c) Scan window too large

3.1.2 S
 can Area

Additionally, the width of the scan window can be adapted to show as much
of the brain parenchyma as possible and to avoid artefacts (Fig. 3.4).
3.1 Settings 27

Fig. 3.3 (continued)

Fig. 3.4 Variation in scan width on coronal ultrasound scans in a preterm infant
with PHVD. (a) Scan width too small, not possible to assess the periventricular white
matter. (b) Increase of scan width improves visualisation of the white matter.
(c) Further increase of scan width, now a little too wide with artefacts (especially on
right side)
28 3 Performing Cranial Ultrasound Examinations

Fig. 3.4 (continued)

3.1 Settings 29

3.1.3 G
 ain

The gain can be adjusted to adapt the overall brightness of the image and to
avoid too bright or too dark images. Time gain compensation can be used
to adjust the gain in specific areas of the image, i.e. superficial and deeper
structures (Fig. 3.5).

Fig. 3.5 Coronal ultrasound in a preterm infant with adaptation of gain and time gain com-
pensation. (a) Gain too low, CUS image becomes too dark. (b) Increasing gain produces
adequate brightness of the image. (c) Further increase of gain, image now too bright. (d)
Adaptation of time gain compensation with near field of image being too bright and
brighter than far field. Time gain compensation should be adjusted to produce equal
reflections from nearby and far-field structures (as in b)
30 3 Performing Cranial Ultrasound Examinations

Fig. 3.5 (continued)

3.1 Settings 31

3.1.4 T
 ransducer Frequency

As mentioned in Chap. 2, neonatal CUS images are obtained with a high-­

frequency micro convex transducer. This enables the most optimal visualisa-
tion of the supratentorial structures. Further increase of transducer frequency
can improve the near-field resolution of superficial structures and optimise
image quality in preterm infants with small heads. In larger infants or when
visualising deeper structures, a lower transducer frequency may be required to
provide sufficient penetration (Figs. 3.6 and 3.7, see Figs. 2.5 and 2.6). For prac-
tical reasons, we therefore advise to have at least two standard presets available
for CUS, one for the preterm infant and one for the larger (near) term infant.

Fig. 3.6 Coronal ultrasound scan (a) and right parasagittal scan (b) in a preterm infant
performed with a transducer frequency of 10 MHz and focus point aimed at the peri-
ventricular regions, showing abnormal asymmetrical echogenicity around temporal
horn of the right ventricle (arrow) on the coronal image (a) which is not clearly delin-
eated on the parasagittal image (b). (c, d) Same images as in (a, b) but now with a
transducer frequency of 8 MHz and the focus point aimed at the temporal region.
Clearly showing the area of abnormal echogenicity both on the coronal (c) and the
parasagittal (d) image (arrows)
32 3 Performing Cranial Ultrasound Examinations

Fig. 3.6 (continued)

3.1.5 F
 ocus Point

Apart from adapting transducer frequency, the focus point can be adjusted
to improve image quality (see Fig. 3.6). At the depth of the focus point, the
ultrasound beam is the narrowest and this improves the resolution. The
focus point should therefore be positioned at or just below the area of inter-
3.1 Settings 33

Fig. 3.6 (continued)

Fig. 3.7 Ultrasound images of an infant, born at 36 weeks of gestation after elective
caesarean section and admitted because of respiratory distress syndrome. (a) Coronal
image showing abnormal echogenicity adjacent to the frontal horn of the right ven-
tricle due to periventricular venous infarction. (b) Same view as in (a) but now with a
high-frequency linear transducer, showing the abnormality in more detail. (c) Right
and left parasagittal views showing the abnormal echogenicity in the right periven-
tricular white matter. Also echogenic lining of the posterior horn of the right lateral
ventricle, probably caused by previous IVH
34 3 Performing Cranial Ultrasound Examinations

Fig. 3.7 (continued)

3.2 Anterior Fontanelle Views 35

est. Most modern transducers have multiple focus points. This improves
resolution over a larger area of the brain. However, when increasing the
number of focus points, the frame rate decreases, and this can lead to slower
processing of the CUS images.

3.2 Anterior Fontanelle Views

For a standard CUS procedure, the anterior fontanelle is used as the acous-
tic window. Images are recorded in at least six standard coronal and five
standard sagittal planes. These standard planes and the anatomical struc-
tures visualised in these planes are presented in Part II.
In addition to the standard planes, the whole brain should be scanned
to obtain an overview of the brain’s appearance. This allows assessment of
the anatomical structures and detection of subtle changes and small and/
or superficially located lesions. Besides the standard views, for any sus-
pected abnormality, images should be recorded in two planes (Figs. 3.6,
3.7, and 3.8).

Fig. 3.8 (a) Coronal and (b) parasagittal CUS scan in a full-term neonate showing uni-
laterally increased echogenicity in the basal ganglia on the right side, representing a
middle cerebral artery perforator stroke (lenticulostriate infarction)
36 3 Performing Cranial Ultrasound Examinations

Fig. 3.8 (continued)

3.2.1 C
 oronal Planes

The anterior fontanelle is palpated, and the transducer is positioned in the

middle of the fontanelle in a way that the left side of the brain will be pro-
jected on the right side of the monitor and vice versa (Fig. 3.9). The probe is
subsequently angled sufficiently forwards and backwards to scan the entire
brain from the frontal lobes at the level of the orbits to the posterior parietal
and occipital lobes (see Part II).

3.2.2 S
 agittal Planes

The transducer is again positioned in the middle of the anterior fontanelle

but now rotated 90° with the marker pointing towards the baby’s mid-face.
The anterior part of the brain will be projected on the left side of the moni-
tor (Fig. 3.10). First, a good view of the midline is obtained. The transducer
is subsequently angled sufficiently to the right and the left to scan out to the
Sylvian fissure and insula on both sides (see Part II). Because the lateral
ventricles fan out posteriorly, the transducer should be positioned with the
3.2 Anterior Fontanelle Views 37

Fig. 3.9 Coronal ultrasound scanning through the anterior fontanelle in a very pre-
term infant. (a) Probe position for obtaining coronal views. (b) Ultrasound image of a
coronal section at the level of the fourth coronal plane (see also Part II). The right side
of the brain is projected on the left side of the image and vice versa
38 3 Performing Cranial Ultrasound Examinations

Fig. 3.10 Sagittal ultrasound scanning through the anterior fontanelle in a very pre-
term infant. (a) Probe positioning for obtaining sagittal views. (b) Midsagittal and (c)
right parasagittal views. The anterior part of the brain is projected on the left side of
the image. The arrow indicates the body marker
3.3 Supplemental Acoustic Windows 39

Fig. 3.10 (continued)

back part slightly more lateral than the front part. The second and fourth
parasagittal planes enable visualisation of, respectively, the right and left lat-
eral ventricle over its entire length (see Fig. 3.10 and Part II). The third and
fifth parasagittal planes show the insula (see Part II).
While scanning in the sagittal planes, it is important to mark which side
of the brain is visualised. This can be done by using the body marker appli-
cation or by an annotation (see Fig. 3.10).

3.3 S
 upplemental Acoustic Windows

If only the anterior fontanelle is used as an acoustic window, deeper brain

structures further away from this fontanelle may not be sufficiently visual-
ised. Lower scan frequencies will enable deeper penetration (see Figs. 2.5,
2.6 and 3.6), but detailed information is lost. Better visualisation can be
obtained by scanning through acoustic windows (Fig. 3.11, see also Part II)
that are closer to these structures, thus allowing the use of higher-frequency,
high-­resolution transducers and visualisation from different angles.
40 3 Performing Cranial Ultrasound Examinations

Fig. 3.11 The acoustic windows. AF anterior fontanelle, PF posterior fontanelle, MF

mastoid (or posterolateral) fontanelle, TW temporal window

The views thus obtained and the anatomical structures visualised are
presented in Part II. In order to avoid excessive manipulation of the infant,
it is recommended to use only those acoustic windows that are easily acces-
sible (i.e. if the infant is positioned on its left side, only the right-sided win-
dows are used and vice versa). The examination can be continued when the
infant is in another position.
Indications for CUS using supplemental windows are presented in the
Appendix.
3.3 Supplemental Acoustic Windows 41

3.3.1 P
 osterior Fontanelle

The posterior fontanelle, located between the parietal and occipital bones
(see Fig. 3.11), enables a good view of the occipital horns of the lateral ven-
tricles, the occipital and temporal parenchyma and the posterior fossa
structures. Using this fontanelle, the posterior fossa can be visualised in the
coronal and sagittal planes. The posterior fontanelle is palpated and the
transducer placed in the middle of the fontanelle in a horizontal position to
obtain a coronal plane (Fig. 3.12) and rotated 90° to the vertical position to
obtain a sagittal plane (Fig. 3.13). Scanning through the posterior fontanelle
enables more accurate detection of haemorrhage in the occipital horns of
the lateral v­ entricles, injury to the occipital and temporal lobes, cerebellar
haemorrhage (CBH) and posterior fossa malformations (Figs. 3.14 and
3.15).

Fig. 3.12 Posterior fontanelle, coronal ultrasound scan in a very preterm infant. (a)
Probe positioning to obtain coronal views. (b) Superior coronal view showing occipital
horns of the lateral ventricles, choroid plexus, occipital lobes, temporal lobes and mes-
encephalon. (c) Inferior coronal view showing occipital lobes with calcarine fissure,
area of tentorium, cerebellar hemispheres, cisterna magna (see Part II Fig.12.4)
42 3 Performing Cranial Ultrasound Examinations

Fig. 3.12 (continued)

3.3 Supplemental Acoustic Windows 43

Fig. 3.13 Posterior fontanelle, sagittal ultrasound scan in a very preterm infant. (a) Probe
positioning to obtain sagittal views. (b) Midsagittal view showing occipital lobe, cerebellar
vermis, aqueduct, fourth ventricle, cisterna magna, quadrigeminal cistern, brain stem and
posterior part of corpus callosum. (c) Parasagittal view showing the occipital lobe, lateral
ventricle with choroid plexus, calcarine fissure, thalamus (see Part II Figs.12.7 and 12.8)
44 3 Performing Cranial Ultrasound Examinations

Fig. 3.13 (continued)

Fig. 3.14 Full-term infant. CUS at 2 weeks, posterior fontanelle views. (a) Coronal view
showing abnormal asymmetrical echogenicity of the left occipital lobe and loss of nor-
mal demarcation of gyri and sulci (arrow). (b) Left parasagittal view, also showing the
abnormal echogenicity of the left occipital lobe (arrow). Compare with (c) normal right
parasagittal view. Diffusion-weighted (d) and T2-weighted (e) MR images at 2 weeks
confirming a left posterior cerebral artery infarction
3.3 Supplemental Acoustic Windows 45

Fig. 3.14 (continued)

46 3 Performing Cranial Ultrasound Examinations

Fig. 3.14 (continued)

e
3.3 Supplemental Acoustic Windows 47

Fig. 3.15 Preterm infant, with bilateral grade 3 IVH and posthaemorrhagic ventricular
dilatation. CUS at 8 days, posterior fontanelle views. (a) Midsagittal view showing
dilated fourth ventricle (blue asterisk) with displacement of cerebellar vermis (arrow)
and widening of the aqueduct (green asterisk). (b) Left parasagittal view showing the
severely dilated occipital horn of the ventricle, filled with haemorrhagic clot
48 3 Performing Cranial Ultrasound Examinations

3.3.2 Temporal Windows

Good transverse views of the brain stem can be obtained through the t­ emporal
window (see Fig. 3.11). The transducer is placed above the ear, approximately
1 cm above and anterior to the external auditory meatus, in a horizontal posi-
tion (Fig. 3.16). The transducer position is subsequently adjusted until visuali-
sation of the brain stem is obtained (Fig. 3.16). The image quality in this view
depends on the bony thickness. Scanning through the temporal window
allows Doppler flow measurements in the circle of Willis (Fig. 3.17), visualisa-
tion of the aqueduct and basal cisterns and d ­ etection of brain stem abnor-
malities. In addition, it can show dilatation of the ventricular system (third
and fourth ventricle and temporal horns) and aqueduct (Fig. 3.18).

Fig. 3.16 Temporal window. (a) Probe positioning. (b–d) Ultrasound scan in a very pre-
term infant performed with micro convex transducer. (b) Normal transverse view
showing mesencephalon (arrow) with aqueduct (green asterisk), upper part of the cer-
ebellum (green arrow), temporal lobes and temporal horn. (c) Same view as in (b) but
with more detail due to the use of the high-frequency linear transducer. (d) Linear
transducer, now angled slightly with detailed views of mesencephalon (arrow), third
ventricle (asterisk) and aqueduct (green asterisk). See Part II Fig. 13.3
3.3 Supplemental Acoustic Windows 49

Fig. 3.16 (continued)

50 3 Performing Cranial Ultrasound Examinations

Fig. 3.16 (continued)

Fig. 3.17 Temporal window. Transverse view of brain stem showing circle of Willis,
using colour Doppler (see also Chap. 9 and Part II Fig. 13.3)
3.3 Supplemental Acoustic Windows 51

Fig. 3.18 Temporal window. Ultrasound scan in same preterm infant with PHVD as in
Fig. 3.15, showing a dilated third ventricle filled with clot (arrow), dilated temporal
horns (green arrow) and also a clot in a dilated fourth ventricle (asterisk)

3.3.3 M
 astoid Fontanelles

The mastoid fontanelles are located at the junction of the temporal, occipital
and posterior parietal bones (see Fig. 3.11). These windows allow visualisa-
tion of the posterior fossa and the midbrain in two planes. After the auricle
is gently bent forward, the transducer is placed behind the ear, just above
the tragus, and subsequently moved until a good view of the posterior fossa
is obtained. Coronal views are obtained with the transducer in a vertical
direction (Fig. 3.19). Transverse (also called axial) planes are obtained with
the transducer in a horizontal position (Fig. 3.20; see also Part II).
Use of the mastoid fontanelle as an additional acoustic window enables
detection of congenital anomalies and haemorrhages in these areas, in par-
ticular cerebellar hypoplasia, CBH, extra axial posterior fossa haemorrhage
and dilatation of the third and fourth ventricles (Figs. 3.21 and 3.22). In our
experience, also ischaemic and infectious cerebellar injury can be detected
using the mastoid fontanelles (Fig. 3.23). It is also a good window for mea-
suring the transverse cerebellar diameter. This is an important measure-
ment and useful for estimating the GA of the neonate.
52 3 Performing Cranial Ultrasound Examinations

Fig. 3.19 Mastoid fontanelle views in a very preterm infant. (a) Probe positioning to
obtain coronal views. (b) Coronal view showing the cerebellum, cisterna magna, mes-
encephalon aqueduct and temporal lobes (see also Part II Fig. 14.3)
3.3 Supplemental Acoustic Windows 53

Fig. 3.20 Mastoid fontanelle views in a very preterm infant. (a) Probe positioning to
obtain transverse (axial) views. (b) Transverse view of the cerebellum, fourth ventricle
and cisterna magna (see also Part II Fig. 14.6)
54 3 Performing Cranial Ultrasound Examinations

Fig. 3.21 Coronal (a) and transverse (b) mastoid fontanelle views in a preterm infant of
28 weeks gestation with a mitochondrial disorder and cerebellar hypoplasia. Note
measurement of transcerebellar diameter, being too small for the gestational age. (c)
Coronal mastoid fontanelle view in a preterm infant of 32 weeks gestation with a
­unilateral hypoplasia of the left cerebellar hemisphere
3.3 Supplemental Acoustic Windows 55

Fig. 3.21 (continued)

Fig. 3.22 Preterm neonate with CBH. Coronal images using right (a) and left (b) mas-
toid fontanelle as acoustic window, showing haemorrhage in left cerebellar hemi-
sphere (arrows)
56 3 Performing Cranial Ultrasound Examinations

Fig. 3.22 (continued)

Fig. 3.23 Ischaemic cerebellar injury in a full term infant with GBS meningitis.
Transverse mastoid fontanelle view shows increased echogenicity of the cerebellar
hemispheres with loss of the normal appearance of fissures and foliation (compare
with Part II Fig. 14.6g)
3.3 Supplemental Acoustic Windows 57

Anterior fontanelle CUS Supplemental acoustic windows

• Standard acoustic window • Posterior fontanelle (occipital
(supratentorial structures) parenchyma, occipital horns,
• Scan the whole brain from frontal posterior fossa)
to occipital and right to left • Temporal window (temporol
• Record at least six standard lobe and horn, midbrain, circle of
coronal and five standard (para) Willis, flow measurements)
sagittal planes • Mastoid fontanelle (midbrain,
• Record (suspected) posterior fossa, ventricular
abnormalities in two planes system)

 ppendix: Indications for Scanning Through

A
Supplemental Windows

Preterm infants (gestational age < 30 weeks):

• Around the third day (CBH?)

• Complicated medical course with circulatory and/or respiratory insta-
bility requires additional scanning
• Around term age (to evaluate cerebellar development) in extremely pre-
term infants or in case of supratentorial brain injury

Both preterm and full-term infants:

• IVH (blood in occipital horns and/or fourth ventricle? Concomitant

CBH?)
• Suspected posterior fossa haemorrhage on standard CUS
• Ventricular dilatation of unknown cause
• (Antenatal) suspected posterior fossa abnormalities
• Congenital malformations
• (Suspected) metabolic disease
• Hypoxic-ischaemic brain injury
• Unexplained neurological symptoms
• Flow velocity measurement in circle of Willis
58 3 Performing Cranial Ultrasound Examinations

Further Reading

Correa F et al (2004) Posterior fontanelle sonography: an acoustic window into the neo-
natal brain. AJNR Am J Neuroradiol 25:1274–1282
Ecury-Goossen GM, Camfferman FA, Leijser LM, Govaert P, Dudink J (2015) State of the
art ultrasound imaging in neonates. J Vis Exp:e52238
Enriquez G et al (2006) Mastoid fontanel approach for sonographic imaging of the new-
born brain. Pediatr Radiol 36(6):532–540
Di Salvo DN (2001) A new view of the neonatal brain: clinical utility of supplemental
neurologic US imaging windows. Radiographics 21:943–955
Steggerda SJ, van Wezel-Meijler G (2016) Cranial ultrasound of the immature cerebellum:
role and limitations. Semin Fetal Neonatal Med 21(5):295–304
Steggerda SJ et al (2009) Neonatal cranial ultrasonography: how to optimize its perfor-
mance. Early Hum Dev 85:93–99
Steggerda SJ et al (2015) Posterior fossa abnormalities in high-risk term infants: compari-
son of ultrasound and MRI. Eur Radiol 25:2575–2583
van Wezel-Meijler G, Steggerda SJ, Leijser LM (2010) Cranial ultrasonography in neo-
nates: role and limitations. Semin Perinatol 34(1):28–38
 4 Assessing Cranial Ultrasound
Examinations

4.1 A
 ssessing Cranial Ultrasound Examinations

When performing and assessing CUS examinations, the anatomy (see Part
II) and maturation (see Chap. 8) of the brain are evaluated, and signs of
pathology, whether congenital or acquired, are sought. In general, anoma-
lies should be visualised in at least two different planes (see Fig. 3.8). A
detailed overview of brain pathology as can be visualised by CUS is provided
in the Atlas on Cranial Ultrasonography by Govaert and de Vries [1].

4.1.1 A
 Systematic Approach for Detecting Cerebral Pathology

Before the CUS scans are assessed for pathology, the quality of the images
should be ascertained (see Chap. 3). (Suspected) abnormalities should be
visible in at least two planes. If an abnormality is only seen in one plane, it
may be an artefact or anamorphosis.
While looking for anomalies, a systematic approach is recommended.
The following can be used as a guideline:

• Are the anatomical structures distinguishable, and do they appear nor-

mal? (see Part II)
• Does the maturation of the brain (cortical folding) appear appropriate
for gestational age (GA)? (see Chap. 8; Fig. 4.1)
• Is there a normal distinction between the cortex and the white ­matter?
(Fig. 4.2)
• Does the cortex appear normal? (Fig. 4.3 see also Fig. 3.14)

© Springer Nature Switzerland AG 2019 59

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
60 4 Assessing Cranial Ultrasound Examinations

Fig. 4.1 (a, b) Coronal ultrasound scans obtained in a full-term (a) and a very preterm
(GA 25+1 weeks) neonate (b) at the level of the bodies of the lateral ventricles. Note the
advanced cortical folding in the full-term infant as compared to the very preterm
infant. Also note the open Sylvian fissures (green arrow) and the very smooth inter-
hemispheric fissure (arrow) in the very preterm infant
4.1 Assessing Cranial Ultrasound Examinations 61

Fig. 4.2 CUS scans in a normal full-term neonate (a, b) and in a full-term neonate with
hypoxic-ischaemic brain injury (c, d). (a) and (c) coronal scans through the trigones of
the lateral ventricles, (b) and (d) parasagittal scans through the insula. (a) and (b) show
normal, hypo-echogenic cortex (arrows) and distinction between cortex and white
matter. (c) and (d) show loss of normal grey-white matter differentiation with blurring
of the cortex, also diffusely increased echogenicity and loss of the normal anatomical
architecture (“fuzzy brain”)
62 4 Assessing Cranial Ultrasound Examinations

Fig. 4.2 (continued)

4.1 Assessing Cranial Ultrasound Examinations 63

Fig. 4.3 Midsagittal ultrasound scans in (a) a normal full-term neonate and (b) a neo-
nate with hypoxic-ischaemic brain injury, showing a broadened cortical rim (arrows),
indicating cortical swelling
64 4 Assessing Cranial Ultrasound Examinations

• Is the echogenicity of the periventricular and subcortical white matter

normal and homogeneous? (Fig. 4.4)
• Is the echogenicity of the thalami and basal ganglia normal and homo-
geneous? (Fig. 4.5)
• Do the size, width, lining and echogenicity of the ventricular system
appear normal? (Figs. 4.6 and 4.7)

Fig. 4.4 (a–d) CUS in a preterm infant born at 25 weeks of GA, scanned at 4 weeks of
age, showing physiological echogenicity (arrows) of the periventricular white matter,
being subtle, mainly homogeneous and less echogenic than the choroid plexus. (a, b)
Coronal views through, respectively, the trigone of the lateral ventricles and the
parieto-­occipital lobes, (c, d) parasagittal views through, respectively, the lateral ven-
tricle and the insula. In (a) linear echogenicity is seen running parallel to the lateral
ventricles, being a physiological phenomenon (green arrow). Also note an echogenic
area in (a) (arrowhead), representing an artefact (only seen in one image direction). In
(a) and (c), the choroid plexus is inhomogeneous. This can be a normal finding at this
age. (e–h) Preterm infant, born at 34 weeks of gestation after a monochorionic twin
pregnancy complicated by intrauterine fetal demise of the co-twin. CUS on 2nd post-
natal day shows inhomogeneously increased echogenicity of the periventricular white
matter with some small focal areas (arrows) of more seriously increased echogenicity:
pathological periventricular echogenicity (PVE). (i) (coronal) and (j) (parasagittal) CUS
in preterm neonate, GA 31+2 weeks, born as second of dichorionic twins; respiratory
failure, showing seriously increased and inhomogeneous echogenicity of the parietal
periventricular white matter: pathological PVE indicating white matter injury
4.1 Assessing Cranial Ultrasound Examinations 65

Fig. 4.4 (continued)

66 4 Assessing Cranial Ultrasound Examinations

Fig. 4.4 (continued)

4.1 Assessing Cranial Ultrasound Examinations 67

Fig. 4.4 (continued)

68 4 Assessing Cranial Ultrasound Examinations

Fig. 4.4 (continued)

4.1 Assessing Cranial Ultrasound Examinations 69

Fig. 4.4 (continued)

70 4 Assessing Cranial Ultrasound Examinations

Fig. 4.5 (a, b) CUS scan in preterm infant (GA 24+3 weeks, scanned on first postnatal
day) showing subtle, diffuse echogenicity of the basal ganglia (arrows). (a) Coronal
view through the frontal horns of the lateral ventricles and (b) parasagittal view
through the left lateral ventricle. This subtle, diffuse echogenicity of the basal ganglia
is a normal finding in very preterm neonates until term equivalent age. Also note the
irregular choroid plexus in (b) (green arrow); this may be a normal finding in very pre-
term neonates. (c, d) Full-term neonate with severe hypoxic-ischaemic brain injury. (c)
Coronal view through the bodies of the lateral ventricles and (d) parasagittal view
through the right lateral ventricle, showing increased echogenicity in the basal gan-
glia (arrow in d) and thalami (green arrows). In (near)-term neonates, this indicates
deep grey matter injury. Also showing broadened cortical rim (arrowhead) and dif-
fusely increased echogenicity (compare with normal images in Figs. 4.1a and 4.2b). (e)
Coronal and (f) parasagittal CUS scan in a preterm neonate (GA 25+2 weeks) who suf-
fered a severe antenatal incident, showing locally and seriously increased echogenicity
in the thalami (arrow), representing thalamic injury. (g) Coronal and (h) parasagittal
CUS scan in full-term neonate showing unilaterally increased echogenicity in the basal
ganglia on the right side (arrow), representing a middle cerebral artery perforator
stroke (lenticulostriate infarction) (same figure as Fig. 3.8). (i, j) Coronal, respectively
parasagittal CUS scan, 4 weeks after birth in a very preterm neonate, GA 26+5 weeks,
showing linear echogenicity in the lenticulostriate vessels on the right side (arrow-
head): so-called lenticulostriate vasculopathy (LSV)
4.1 Assessing Cranial Ultrasound Examinations 71

Fig. 4.5 (continued)

72 4 Assessing Cranial Ultrasound Examinations

Fig. 4.5 (continued)

4.1 Assessing Cranial Ultrasound Examinations 73

Fig. 4.5 (continued)

74 4 Assessing Cranial Ultrasound Examinations

Fig. 4.5 (continued)

4.1 Assessing Cranial Ultrasound Examinations 75

Fig. 4.5 (continued)

76 4 Assessing Cranial Ultrasound Examinations

Fig. 4.6 (a, b) Normal CUS scan in very preterm neonate (GA 25 weeks), performed on
the first postnatal day, shortly after birth. (a) Coronal view at the level of the frontal
horns of the lateral ventricles, (b) parasagittal scan through the right lateral ventricle.
Note the subtle, physiological echogenicity of the parietal white matter (arrow). Also
note the large, bulky choroid plexus (green arrow): a normal finding at this age. (c) and
(d) Coronal and parasagittal views in the same infant, 3 h later, now showing echo-
genic areas in the frontal horns of the lateral ventricles and in the left temporal horn
(arrow), representing bilateral IVH. Also note irregular echogenicity in the left cerebel-
lar hemisphere (green arrow in c), representing CBH. (e) Coronal, (f) midsagittal and (g)
parasagittal CUS in a very preterm infant (GA 27+4 weeks) with PHVD, performed 8 days
after birth, showing dilatation of the lateral ventricles, 3rd (arrows in e and f) and 4th
(green arrow in f) ventricle, and echogenic ventricular lining (arrowheads in e and g).
Also note the blood clot in the right frontal horn (red arrow in e) and the echogenicities
in the cavum septum pellucidum (red arrow in f) and in the occipital and temporal
horns (red arrows in g), representing haemorrhage
4.1 Assessing Cranial Ultrasound Examinations 77

Fig. 4.6 (continued)

78 4 Assessing Cranial Ultrasound Examinations

Fig. 4.6 (continued)

4.1 Assessing Cranial Ultrasound Examinations 79

Fig. 4.6 (continued)

80 4 Assessing Cranial Ultrasound Examinations

e e e
e

Fig. 4.7 Same preterm infant as Fig. 4.6e–g, 9 days later. Thanks to repetitive lumbar taps
to prevent increased intracranial pressure, the ventricular dilatation has improved. (a)
Coronal CUS scan at the level of the frontal horns of the lateral ventricles: measurements of
the ventricular index (VI) (arrow) according to Levene and of the anterior horn width (AHW)
(green arrow) according to Davies on both sides. (b) Parasagittal scan through the left lat-
eral ventricle: measurement of the thalamo-occipital distance (TOD) according to Davies
4.1 Assessing Cranial Ultrasound Examinations 81

Fig. 4.8 (a–c) a Coronal at the level of the trigone of the lateral ventricles and b para-
sagittal CUS scan in a very preterm infant scanned at term equivalent age, showing
enlarged subarachnoidal space (arrows), widening of interhemispheric fissure (green
arrow) and somewhat plump gyri (reduced complexity of gyral folding) (arrow head),
indicating volume loss. Compare with normal full-term neonate (Fig. 4.2a and b)
82 4 Assessing Cranial Ultrasound Examinations

Fig. 4.9 Coronal CUS scan at the level of the frontal horns of the lateral ventricles in a
very preterm neonate (GA 27 weeks), showing a massive left-sided IVH with periven-
tricular haemorrhagic infarction (PVHI) (arrow) and a midline shift to the right side
• In the case of ventricular enlargement, the lateral ventricles are mea-
sured according to standard guidelines (Fig. 4.7) (Levene [2], Davies
et al. [3], Brouwer et al. [4]; see also Appendix).
• Are the widths of the subarachnoidal spaces appropriate for age (Fig. 4.8)?
• Is there a midline shift (Fig. 4.9)?

Image assessment
Anatomy
Maturation
Distinction cortex/white matter
Cortex
Periventricular and subcortical white matter
Thalami and basal ganglia
Ventricular system
Measurements
Subarachnoidal spaces
Midline shift?
References 83

Appendix: Measurement of the Lateral Ventricles

• Ventricular index (VI): the distance between the midline and the lateral
wall of the anterior horn (coronal plane) [2] (see Fig.4.7a)
• Anterior horn width (AHW): the diagonal width of the anterior horn
measured at its widest point (coronal plane) [3] (see Fig.4.7a)
• Thalamo-occipital distance (TOD): the distance between the thalamus
and the outer border of the occipital horn (parasagittal plane) [3] (see
Fig. 4.7b)

In the third coronal plane (at the level of the interventricular foramina of
Monro), the ventricular width is measured on both the left and the right
side by measuring the distance from the lateral wall of the ventricle to the
midline. Reference values are available [4] (Fig. 4.7).
The width of the anterior horn of the lateral ventricles (AHW) is mea-
sured in the third coronal plane (at the level of the interventricular foramina
of Monro). The width is measured on each side as the distance between the
medial wall and the floor of the lateral ventricle at the widest point.
Reference values are available [4] (Fig. 4.7a).
In the second and fourth parasagittal planes, the TOD is measured on
each side as the distance between the outermost point of the thalamus at its
junction with the choroid plexus and the outermost part of the occipital
horn. Reference values are available [4] (Fig. 4.7b).

References

1. Govaert P, De Vries LS (2010) An atlas of neonatal brain sonography, 2nd edn.

MacKeith Press, Cambridge
2. Levene MI (1981) Measurement of the growth of the lateral ventricles in preterm
infants with real-time ultrasound. Arch Dis Child 56:900–904
3. Davies MW et al (2000) Reference ranges for the linear dimensions of the intracranial
ventricles in preterm neonates. Arch Dis Child Fetal Neonatal Ed 82:F218–F223
4. Brouwer MJ et al (2012) New reference values for the neonatal cerebral ventricles.
Radiology 262:224–233
84 4 Assessing Cranial Ultrasound Examinations

Further Reading

Boxma A et al (2005) Sonographic detection of the optic radiation. Acta Paediatr

94:1455–1461
Daneman A, Epelman M (2015) Neurosonography: in pursuit of an optimised examina-
tion. Pediatr Radiol 45:S406–S412
de Goederen R et al (2017) Effect of preterm birth on echogenicity in basal ganglia.
Ultrasound Med Biol 43:2192–2199
de Vries LS et al (1992) The spectrum of leukomalacia using cranial ultrasound. Behav
Brain Res 49:1–6
Ecury-Goossen GM et al (2015) State of the art cranial ultrasound imaging in neonates.
J Vis Exp (96):e52238
Fabre C et al (2018) Hyperechogenicity of lenticulostriate vessels: a poor prognosis or a
normal variant? A seven year retrospective study. Pediatr Neonatol
Griffiths PD et al (2010) Atlas of foetal and postnatal brain MRI. Mosby Elsevier,
Philadelphia, PA
Horsch S et al (2005) Ultrasound diagnosis of brain atrophy is related to neurodevelop-
mental outcome in preterm infants. Acta Paediatr 94(12):1815–1821
Leijser LM et al (2006) Using cerebral ultrasound effectively in the newborn infant. Early
Hum Dev 82(12):827–835
Leijser LM et al (2009) Frequently encountered cranial ultrasound features in the white
matter of preterm infants: correlation with MRI. Eur J Paediatr Neurol. 13:317–326
Leijser LM et al (2010) Lenticulostriate vasculopathy in very preterm infants. Arch Dis
Child Fetal Neonatal Ed 95:F42–F46
Meijler et al (2016) Neonatal cranial ultrasonography. Diagnostic pediatric ultrasound. 1st
edn. Beek and Van Rijn
Murphy et al (1989) Cranial ultrasound assessment of gestational age in low birthweight
infants. Arch Dis Child 64:569–572
Naidich TP et al (1994) The developing cerebral surface. Preliminary report on the pat-
terns of sulcal and gyral maturation—anatomy, ultrasound, and magnetic resonance
imaging. Neuroimaging Clin N Am 4:201–240
Sie LT et al (2000) Early MR features of hypoxic-ischaemic brain injury in neonates with
periventricular densities on sonogram. Am J Neuroradiol 21:852–861
Shin HJ et al (2015) Imaging patterns of sonographic LSV and correlation with clinical
and neurodevelopmental outcomes. J Clin Ultrasound 43:367–374
Steggerda SJ et al (2009) Neonatal cranial ultrasonography: how to optimise its perfor-
mance. Early Hum Dev 85:93–99
van Wezel-Meijler G, de Vries LS (2014) Cranial ultrasound—optimising utility in the
NICU. Curr Pediatr Rev 10(1):16–27
van Wezel-Meijler G et al (2011) Diffuse hyperechogenicity of basal ganglia and thalami
in preterm neonates: a physiologic finding? Radiology 258(3):944–950
 5 Timing of Ultrasound Examinations

5.1 T
 iming of Ultrasound Examinations

To obtain optimal information from CUS serial, carefully timed examina-

tions are essential, in both preterm and in sick full-term infants. If timing is
not optimally chosen, time intervals between CUS examinations are too
long, or CUS examinations are discontinued too early, important informa-
tion and/or injury may be missed. On the other hand, if the quality of CUS
is good, timing is well chosen, proper transducers are used and, in the case
of preterm birth, serial examinations are continued until term equivalent
age (TEA); most clinically relevant abnormalities will be detected.
Serial CUS is not only essential for accurate and reliable detection of
brain injury, it also enables follow-up of brain growth and maturation, tim-
ing of injury and following lesions over time.

5.1.1 U
 ltrasound Screening

In neonatal units it is useful to apply general guidelines for CUS examina-

tions (see Chaps. 3 and 4) and a CUS screening schedule. Schedules may
considerably vary between neonatal units. In Appendix 5.1 an adaptation
from the national guidelines of the Dutch Pediatric Society for CUS screen-
ing in preterm and high-risk full-term neonates is presented. These guide-
lines are based on results of several neuroimaging studies examining the
performance of CUS, and take the following into account:

© Springer Nature Switzerland AG 2019 85

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
86 5 Timing of Ultrasound Examinations

• A first CUS examination soon after birth can give information on brain
maturation, congenital anomalies of the brain, congenital infections,
some metabolic disorders, traumatic brain injury and the antenatal
onset of lesions. It may also serve as a baseline and comparison for the
following CUS examinations.
• Haemorrhagic lesions usually become visible within hours after the
incident.
• In neonates most haemorrhagic lesions develop around birth.
• More than 90% of germinal matrix-intraventricular haemorrhages
(GMH-IVH) (see Chap. 6) develop within the first 3 days after birth.
• Most CBH (see Chaps 3 and 6) develop within the first 3 days after birth
or shortly after an acute clinical deterioration (see Fig. 6.10).
• GMH-IVH and CBH often co-exist.
• Extension of GMH usually occurs within the first week after onset.
• PHVD (see Chaps. 4 and 6) tends to develop 7–14 days after the onset of
IVH and thus asks for frequent, sequential scanning in neonates with
IVH, especially in the case of a large haemorrhage, as PHVD may need
treatment (Fig. 5.1; see also Figs. 4.6e–g and 4.7).
• Large CBH (see Chap. 6) may cause destruction of the developing cere-
bellar parenchyma and thus ask for follow-up CUS until TEA (Fig. 5.2).
• It takes a variable period of time (hours to days) before ischaemic
changes become clearly visible (Figs. 5.3, 5.4 and 5.5).
• Especially in preterm infants, the first stages and the milder spectrum of
hypoxic-ischaemic brain injury may be hard to distinguish from normal
(maturational) phenomena occurring in the immature brain (Fig. 5.6,
see also Chap. 8) [1, 2]. An overview how to distinguish normal, physi-
ological PVE in the white matter from pathological PVE is presented in
Appendix 5.2.
• Hypoxic-ischaemic brain injury may evolve over a variable period of
time (hours to weeks). CUS examinations at regular intervals are needed
to assess all stages of hypoxic-ischaemic brain injury and to avoid miss-
ing abnormalities such as non-physiological echodensities and small
cystic lesions as these may be of clinical importance (Fig. 5.7; see Figs. 5.3
and 5.5 and Chap. 6).
5.1 Timing of Ultrasound Examinations 87

Fig. 5.1 Preterm infant, GA 31+4 weeks, perinatal asphyxia, respiratory and circulatory fail-
ure. IVH on first postnatal day, progressing to a bilateral IVH grade III (see Chap. 6) within 2
days. (a, b) On postnatal day 6, CUS (a coronal scan through the frontal horns of the lateral
ventricles, b parasagittal scan through the left lateral ventricle) shows bilateral IVH causing
PHVD. Repetitive cerebrospinal fluid tapping (through lumbar punctures) was performed
to prevent increased intracranial pressure. (c, d) (c coronal scan through the frontal horns
of the lateral ventricles, d parasagittal scan through the right lateral ventricle). Two days later
the ventricular dilatation has significantly improved shortly after a lumbar puncture. The
dotted lines represent measurements of the lateral ventricles (see Chap. 4, Appendix and
Fig. 4.7). (e, f) (e coronal scan through the third ventricle, f parasagittal scan through the
right lateral ventricle). The repetitive lumbar punctures did not lead to stabilisation: prior to
the procedure, there is still marked ventricular dilation. It was therefore decided to place a
ventricular reservoir, which was done 2½ weeks after birth. (g, h) (g coronal scan through
the frontal horns of the lateral ventricles, h parasagittal scan through the right lateral ven-
tricle). Three weeks after placement of the reservoir and repetitive punctures from the res-
ervoir, the ventricular dilatation has improved. Note the reservoir in the lateral ventricle
(arrow). (i–l) (i coronal scan through the body of the lateral ventricles, j coronal scan
through the trigone of the lateral ventricles, k parasagittal scan through the right lateral
ventricle, l parasagittal scan through the right lateral ventricle). At TEA the PHVD has stabi-
lised, CSF taps from the reservoir were no longer necessary and the baby did not need a
permanent drain. (m) Early MRI (coronal T2-weighted scan) at PMA 34 weeks, performed
prior to placement of the ventricular reservoir, shows severe ventricular dilatation, clots in
the lateral ventricles and irregular signal intensity of the white matter (arrows) due to
increased intracranial pressure (courtesy professor Linda de Vries, Wilhelmina Children’s
Hospital, Utrecht)
88 5 Timing of Ultrasound Examinations

Fig. 5.1 (continued)

5.1 Timing of Ultrasound Examinations 89

Fig. 5.1 (continued)

90 5 Timing of Ultrasound Examinations

Fig. 5.1 (continued)

5.1 Timing of Ultrasound Examinations 91

Fig. 5.1 (continued)

92 5 Timing of Ultrasound Examinations

Fig. 5.1 (continued)

5.1 Timing of Ultrasound Examinations 93

Fig. 5.1 (continued)

94 5 Timing of Ultrasound Examinations

Fig. 5.1 (continued) (n–o) TEA MRI

n
(n T1-weighted inversed recovery
image, slightly right from the
midline, o T2-weighted axial image
at basal ganglia level) shows normal
maturation and growth of the brain.
The occipital horn of the right lateral
ventricle is irregularly dilated (arrow
in o); this is probably due to a small
venous infarction at the ipsilateral
side (not shown). Some remnants of
the IVH are still seen (green arrow in
o). The ventricular reservoir is visible
in n

o
5.1 Timing of Ultrasound Examinations 95

Fig. 5.2 Coronal ultrasound scan through the right mastoid fontanelle in a preterm
infant born at 34 weeks of gestation as part of monochorionic twins. Pregnancy was
complicated by twin-to-twin transfusion syndrome and intrauterine fetal demise of
the recipient twin at 20 weeks of gestation. One day later a unilateral haemorrhage in
the right cerebellar hemisphere was diagnosed in the donor twin. On the postnatal
ultrasound scan, the right cerebellar hemisphere (asterisk) is obviously smaller than
the left hemisphere (green asterisk) and has become dysplastic (loss of the normal ana-
tomical features)
96 5 Timing of Ultrasound Examinations

Fig. 5.3 Preterm neonate, GA 32 weeks, intrauterine growth retardation, born after
emergency caesarean section because of fetal distress. Ultrasound scans performed
on postnatal day 1 (a and b) and 10 (c and d), and at 1 month of age (e and f). (a)
Coronal CUS scan at the level of the trigone of the lateral ventricles and (b) parasagittal
CUS scan through the right lateral ventricle initially show physiological echogenicity of
the periventricular white matter being subtle and homogeneous; (c) coronal scan
through the parieto-occipital lobes and (d) parasagittal scan through the insula show
abnormally increased, inhomogeneous echogenicity of the white matter. Cyst forma-
tion was observed around 2 weeks postnatally. After 1 month (e coronal scan through
the frontal horns of the lateral ventricles and f parasagittal scan through the right
insula), extensive cystic lesions have developed (grade cystic periventricluar leukoma-
lacia (c-PVL)) (see Chap. 6). (g) MRI scan (T2-weighted, transverse image at high ven-
tricular level) performed around TEA shows extensive cystic lesions in the frontal white
matter, smaller cystic lesions in the right parieto-occipital area (arrows), loss of white
matter volume, irregular and plump shape of the lateral ventricles and small volume of
the basal ganglia (asterisk). Also showing small IVH on the left side (green arrow)
5.1 Timing of Ultrasound Examinations 97

Fig. 5.3 (continued)

98 5 Timing of Ultrasound Examinations

Fig. 5.3 (continued)

5.1 Timing of Ultrasound Examinations 99

Fig. 5.3 (continued)

100 5 Timing of Ultrasound Examinations

Fig. 5.4 Term neonate, born asphyxiated, with hypoxic-ischaemic encephalopathy.

Coronal (a through body of the lateral ventricles) and parasagittal (b through left lat-
eral ventricle) CUS scan on day 1 shows subtly increased echogenicity in the thalami
(arrow). Also showing slit-like ventricles, loss of the normal anatomical features and
disappearance of sulci, a combination of findings indicating cerebral oedema. Twelve
days later (c and d), the abnormal echogenicity in the thalami is obvious (arrow), and
the thalami appear swollen. Also showing an area of low echogenicity representing
the posterior limb of the internal capsule (asterisk in d) and inhomogeneous echo-
genicity in the parietal white matter (green arrow in d)
5.1 Timing of Ultrasound Examinations 101

Fig. 5.4 (continued)

102 5 Timing of Ultrasound Examinations

Fig. 5.5 Preterm neonate, GA 30+4 weeks, respiratory failure, perinatal infection. CUS
on day 1 (a coronal scan through the trigone of the lateral ventricles and b parasagittal
scan through the lateral ventricle) shows somewhat inhomogeneous echogenicity of
the parietal white matter (arrows). Two days later (c coronal scan through the parieto-
occipital lobes and d parasagittal scan through the right insular area), the echogenicity
of the periventricular white matter is obviously abnormal, being patchy and inhomo-
geneous. At the age of 3 weeks (e and f), cystic lesions are seen in the left parietal
white matter and the echogenicity of the white matter is still patchy and inhomoge-
neous. At TEA (g and h) in addition to the cysts, there are signs of white matter volume
loss: wide extracerebral spaces (arrows) and irregular shape of the lateral ventricle
(green arrow in h). The TEA MRI (i) (T2-weighted transverse image at midventricular
level) confirms the cystic lesions on the left side and additionally shows small cystic
lesions on the right (arrow) that remained undetected with CUS
5.1 Timing of Ultrasound Examinations 103

Fig. 5.5 (continued)

104 5 Timing of Ultrasound Examinations

Fig. 5.5 (continued)

5.1 Timing of Ultrasound Examinations 105

Fig. 5.5 (continued)

106 5 Timing of Ultrasound Examinations

Fig. 5.5 (continued)

i
5.1 Timing of Ultrasound Examinations 107

Fig. 5.6 Coronal (a through frontal lobes) and parasagittal (b through left insular area)
CUS in a very preterm neonate, GA 25 weeks on postnatal day 2, showing subtle, physi-
ological echogenicity in the frontal white matter. Compare with (c and d) preterm neo-
nate (GA 28 weeks), CUS on day 3 showing inhomogeneously increased echogenicity
in the frontoparietal white matter. Coronal (e through frontal horns of lateral ventri-
cles) and parasagittal (f through left lateral ventricle) CUS in extremely preterm neo-
nate (GA 24+3 weeks), showing subtle echogenicity in the basal ganglia (arrow), being
a normal finding in preterm neonates. The CUS images in the 28 weeks GA neonate (g
and h, same infant as in c and d) show abnormally increased and inhomogeneous
echogenicity in the basal ganglia (arrow) and thalamus (green arrow)
108 5 Timing of Ultrasound Examinations

Fig. 5.6 (continued)

5.1 Timing of Ultrasound Examinations 109

Fig. 5.6 (continued)

110 5 Timing of Ultrasound Examinations

Fig. 5.6 (continued)

5.1 Timing of Ultrasound Examinations 111

Fig. 5.7 Coronal (a through parieto-occipital lobes) and parasagittal (b through right
insular area) ultrasound scan in preterm infant (GA 33+3 weeks), performed 8 days after
birth, showing increased and inhomogeneous echogenicity of the parietal-occipital
white matter. (c) Early MRI 1 day later at PMA 34+4 weeks: axial T1-weighted image at
high ventricular level shows multiple punctate white matter lesions in the periven-
tricular white matter. The boy was discharged to a level two hospital where unfortu-
nately no follow-up CUS scans were done. (d) TEA T1-weighted MRI at almost
supraventricular level now shows some small white matter cysts. A few punctate white
matter lesions can still be seen, but most have now disappeared
112 5 Timing of Ultrasound Examinations

Fig. 5.7 (continued)

c

d
5.1 Timing of Ultrasound Examinations 113

• The change from abnormal echogenicity into cystic lesions takes 10–14
days in infants with extensive cysts (grade 3 periventricular
­leukomalacia (PVL)) and may take up to 4–5 weeks in infants with
small, focal cystic lesions (grade 2 PVL) (see Figs. 5.3, 5.5 and 5.7 and
Chap. 6).
• Large and extensive cysts remain visible for several weeks, will usually
become gradually smaller and are often no longer visible on ultrasound
scans after a few months. Instead, ex vacuo dilatation and irregular shape
of the lateral ventricle are seen.
• Localised and smaller cysts are only visible for a few weeks and may not
be visible at TEA. Instead, ex vacuo dilatation and irregular shape of the
lateral ventricle may be seen.
• In preterm infants lesions (especially white matter injury) may develop
throughout the neonatal period, related to postnatal events.
• Small CBH and diffuse white matter injury, frequently encountered in
very preterm neonates, are not well detected with CUS and more reliably
evaluated using MRI (Figs. 5.8 and 5.9).
• Meningitis and other brain infections can have a very rapid, fulminant
course and may lead to infarction or abscess formation with parenchy-
mal destruction and/or impaired cerebrospinal fluid drainage with
hydrocephalus. Infants with these conditions should therefore be
intensively monitored with repetitive CUS (Fig. 5.10; see also
Fig. 2.4a–d).
• A CUS examination performed on the first postnatal day enables detec-
tion of congenital anomalies, antenatally acquired injury and perinatally
acquired haemorrhage.
• CUS examinations repeated during the first week will detect almost
all haemorrhagic lesions and identify their maximum extent and will
enable detection of the acute stages of perinatal hypoxic-ischaemic brain
injury.
• In the case of a large IVH, follow-up scanning over a longer period of
time (2–3 weeks after the initial haemorrhage) is needed for detection of
PHVD.
114 5 Timing of Ultrasound Examinations

Fig. 5.8 Axial (a) and coronal (b) ultrasound scans through the right mastoid fonta-
nelle in preterm infant (GA 28+4 weeks, PMA 33 weeks) show a small area of increased
echogenicity in right cerebellar hemisphere (arrow), suspect for a small haemorrhage.
The axial T2-weighted MRI scan performed at TEA (c) confirms a small haemorrhage
(arrow) in the right cerebellar hemisphere
5.1 Timing of Ultrasound Examinations 115

Fig. 5.8 (continued)

c
116 5 Timing of Ultrasound Examinations

Fig. 5.9 Coronal (a through the trigone of the lateral ventricles) and parasagittal (b
through the right insular area) ultrasound scans in a small for gestational age preterm
infant (GA 26+2 weeks) with a complicated neonatal course. At PMA 31 weeks, the
echogenicity of the periventricular white matter is still inhomogeneous and increased
and the lateral ventricles are wide and irregularly shaped due to white matter volume
loss. At TEA
5.1 Timing of Ultrasound Examinations 117

Fig. 5.9 (continued) (c and d), the extracerebral spaces are wide (arrows) and the
irregular widening of the lateral ventricles (ex vacuo ventricular dilatation), especially
the occipital horns, is more obvious. T1-weighted MRI scan (e) at TEA (high ventricular
level) confirms the white matter volume loss (deep sulci, abutting the ventricles, wide
and irregular lateral ventricles and wide extracerebral spaces), due to diffuse white
matter injury. There are no focal changes in the white matter
118 5 Timing of Ultrasound Examinations

Fig. 5.9 (continued)

e
5.1 Timing of Ultrasound Examinations 119

Fig. 5.10 Coronal (a and b) and parasagittal through the right lateral ventricle (c) ultra-
sound scans in 3-month-old infant who presented with E. coli meningitis at the age of
3 weeks and developed severe hydrocephalus. Despite a ventriculoperitoneal drain in
situ (arrow in b), there is irregular dilatation, mainly of the frontal horns of the lateral
ventricles. Debris is still present in the left lateral ventricle (arrow in a). The sulci appear
broad and echogenic (green arrow in a) and the echogenicity in the parietal white mat-
ter is irregular (red arrows in b and c). (d–j) Preterm infant born at 34 weeks of gestation
after uncomplicated pregnancy and delivery who developed GBS sepsis and meningi-
tis on the 4th postnatal day. (d and e) CUS at postnatal day 7 showing slit-like ventri-
cles, increased and irregular echogenicity of the white matter (arrows) and increased
echogenicity in the left thalamic/basal ganglia region (green arrow in e). From day 12
the baby developed progressive ventricular dilatation which was treated with repeti-
tive lumbar punctures for decompression. (f–h) At 2 weeks of age, CUS shows dilata-
tion of the lateral and third ventricles, echogenic ventricular lining, septation (arrows in
f and g) and debris (green arrow in h) within the lateral ventricle. (i and j) At 5 weeks of
age, the ventricular dilatation has improved, septation is still present in the right fron-
tal horn and there is a cystic lesion in the left thalamus (arrow), surrounded by
increased echogenicity. (k–m) Very preterm infant with Candida sepsis and persisting
positive blood and urine cultures. CUS shows small echogenic lesions in the basal gan-
glia and white matter, suspect for fungal balls. Note the small angle of insonation: in
this case the PA probe was used because of the small size of the anterior fontanelle.
(n–q) Late preterm infant, born at 36 weeks gestation, admitted at 2 weeks of age with
seizures due to enterovirus sepsis/meningitis. CUS at admission (n coronal through
frontal lobes, o parasagittal through right insular area) shows irregular, inhomoge-
neous echogenicity of the periventricular white matter. Follow-up CUS at 8 weeks of
age (p, q) shows cystic degeneration, mainly in the frontal white matter. Some small
cystic lesions are also present in the parietal white matter
120 5 Timing of Ultrasound Examinations

Fig. 5.10 (continued)

5.1 Timing of Ultrasound Examinations 121

Fig. 5.10 (continued)

122 5 Timing of Ultrasound Examinations

Fig. 5.10 (continued)

5.1 Timing of Ultrasound Examinations 123

Fig. 5.10 (continued)

124 5 Timing of Ultrasound Examinations

Fig. 5.10 (continued)

5.1 Timing of Ultrasound Examinations 125

Fig. 5.10 (continued)

126 5 Timing of Ultrasound Examinations

Fig. 5.10 (continued)

5.1 Timing of Ultrasound Examinations 127

Fig. 5.10 (continued)

128 5 Timing of Ultrasound Examinations

Thus:
• Sequential CUS examinations are needed to assess lesions over time and
to distinguish (mild) pathology from normal (maturational) phenomena
[1, 2].
• In preterm infants, sequential CUS examinations throughout the neona-
tal period until TEA are needed to follow brain growth and develop-
ment, to follow brain lesions and to detect later onset of injury.

For infants who were born very prematurely and are later transferred
from the tertiary centre to a local hospital, we recommend to arrange con-
tinuation of CUS examinations. If local facilities are insufficient, it is
­recommended that CUS examinations are performed at the neonatal centre
at least around discharge and/or TEA.

5.1.2 Cranial Ultrasonography at Term-Corrected Age

In infants born very prematurely (GA < 28 weeks) and in infants with (sus-
pected) parenchymal brain injury and/or large IVH, we recommend to per-
form a CUS examination around TEA. This term examination is done to see
the later stages of injury (see Figs. 5.2, 5.3e, f and 5.5g, h), to detect new
lesions that may have developed after discharge and to evaluate brain
growth and development (see Fig. 4.1). CUS at TEA can also add valuable
information regarding the prediction of outcome. The predictive value of
CUS at TEA is comparable to that of conventional MRI at TEA.
CUS examinations performed around TEA may show:

• Cysts in regression, within the spectrum of cystic-PVL (c-PVL) (see Chap. 6)

• Late-onset PVL
• Ex vacuo ventricular dilatation related to volume loss as a result of
white matter injury, often associated with increased width of the sub-
arachnoidal space and widening of the interhemispheric fissure
(Fig. 5.11; see also Fig. 4.10)
• PHVD following a GMH-IVH (see Fig. 5.1 and Chap. 6)
• Cystic phase of PVHI (see Chap. 6) (Fig. 5.11; see also Fig. 6.7f–h)
• Cystic phase of focal arterial infarction (Fig. 5.12)
• Cerebellar atrophy or dysplasia, related to CBH or other posterior fossa
haemorrhages (see Fig. 5.2)
5.1 Timing of Ultrasound Examinations 129

Fig. 5.11 Coronal (a) and parasagittal through the left (b) and the right (c) lateral ven-
tricle and the right insular area (d) ultrasound scans, performed around TEA in a pre-
term infant, GA 26 weeks. Grade 3 IVH, complicated by PHVD and a right-sided
PVHI that has now evolved into a large porencephalic cyst and some smaller cysts (see
also Chap. 6 and Fig. 6.5 [same infant]). Also note the wide extracerebral spaces (arrow
in a) and ventricular dilatation, indicating volume loss
130 5 Timing of Ultrasound Examinations

Fig. 5.11 (continued)

5.1 Timing of Ultrasound Examinations 131

Fig. 5.12 Coronal (a) and parasagittal through the left insular area (b) ultrasound scans
performed at TEA in a moderate preterm infant, born at 34 weeks of gestation, with a
middle cerebral artery infarction, showing cystic degeneration of the infarcted area
132 5 Timing of Ultrasound Examinations

Neonatal CUS examinations Background

• Routine screening schedule in • Haemorrhagic lesions:
neonatal units – Early detection (hours)
• Intensify if (suspected)  – Onset generally <72h after
abnormalities birth
• TEA CUS:  – Extension first days after
– GA ≤ 28 weeks: event
– (Suspected) parenchymal  – Later complications (days/
brain injury, including: weeks)
– non-physiological PVE still • Ischaemic lesions:
present at discharge from  – Later detection (hours/days
NICU after event)
– IVH > grade 2  – May develop any time during
– PHVD the neonatal period
– Posterior fossa haemorrhage  – May become more severe
– Brain infections over a long period (weeks)
 – Late detection of end stages
 – Early stages may seem mild
and may resolve
 – May be difficult to
distinguish from normal
phenomena

Appendix 5.1: Recommendations for CUS Examinations

CUS Indications
CUS is indicated in all neonates at risk of abnormal/delayed brain matu-
ration and/or central nervous system (CNS) abnormalities (congenital or
acquired) and in neonates with neurological symptoms.

1. In relation to pregnancy complications:

(a) Maternal trauma

(b) Complicated monochorionic twin pregnancies (twin-to-twin trans-
fusion syndrome, fetal demise of co-twin, selective intrauterine
growth restriction, twin-anaemia-polycythaemia sequence)
5.1 Timing of Ultrasound Examinations 133

(c) Intrauterine interventions (such as intrauterine transfusions, fetal

surgery)
(d) Antenatal infection
(e) Fetal and neonatal alloimmune thrombocytopenia
(f) (Suspected) antenatal CNS abnormalities
(g) (Suspected) congenital CNS malformations

2. In relation to neonatal conditions:

(a) Preterm birth (GA < 32 weeks)

(b) Birth weight ≤ 2, 3rd centile for GA
(c) Birth weight < 1500 g
(d) Syndrome and/or congenital malformations
(e) After resuscitation
(f) (Hypoxic-ischaemic) encephalopathy
(g) Meningitis/encephalitis
(h) Metabolic disorders
(i) Symptomatic, severe and/or long-lasting hypoglycaemia
(j) Serum bilirubin > exchange transfusion level
(k) Unexplained significant haemoglobin drop
(l) Haemodynamically significant ductus arteriosus after neonatal
surgery
(m) Before and after extracorporeal membrane oxygenation (ECMO)
(n) After clinical deterioration (respiratory failure, circulatory failure,
apnoeic spells, septicaemia, necrotising enterocolitis, etc.)

3. Neurological symptoms:

(a) Seizures
(b) Abnormal tone
(c) Abnormal movements
(d) Encephalopathy
(e) Unexplained apnoeic spells
(f) Unexplained restlessness
(g) Widened skull sutures
(h) Microcephaly (< 2, 3rd centile)
(i) Macrocephaly (> 97th centile)
134 5 Timing of Ultrasound Examinations

Timing of CUS Examinations

Adapted from the National Guidelines on Neonatal Neuro-imaging,
Dutch Paediatric Association 2015.

1. Preterm Neonates

Gestational age (weeks)

24–26 26–28 28–30 30–32 ≥32–37
1st week
Day 1 X X X X When
Day 3 X X X X indicated
Day 7 X X X X and/or if
2nd week X X X X admitted
Afterwards every X X X X to NICU
other weeka
At discharge X X X X
from NICU
At discharge X X When When
home and/or TEA indicated indicated
a
At least until 4th postnatal week in infants <32 weeks GA and until 6th postnatal week
in infants < 28 weeks GA. Afterwards less often in stable infants without abnormalities
on previous CUS scans

This schedule should be intensified in the case of:

• CUS abnormalities seen:

–– GMH-IVH, PHVD, CBH and (suspected) CNS infection at least

every other day until stabilisation
–– Inhomogeneous PVE and c-PVL at least once a week until stabilisation
–– PVHI at least once a week until stabilisation

• Clinical deterioration (respiratory failure, circulatory failure, apnoeic

spells, septicaemia, necrotising enterocolitis, etc.): soon after the inci-
dent, afterwards weekly until 3 weeks after the incident
• Systemic viral infection or viral gastro-enteritis at least weekly until 2
weeks after onset
5.1 Timing of Ultrasound Examinations 135

• Unexplained haemoglobin drop: soon after the incident

• Neonatal surgery procedure: soon after the procedure and at least weekly
thereafter until 3 weeks after the surgery

2. High-risk full-term neonates:

• Acute neurological symptoms: as soon as possible and thereafter depend-
ing on clinical condition and CUS findings
• HIE: at admission, on days 2–3, and after hypothermia treatment
(around day 5)
• (Suspected) parenchymal injury: soon and 3–7 days after insult, thereaf-
ter depending on clinical condition and CUS findings
• (Suspected) metabolic disorder: at admission, thereafter depending on
clinical condition and CUS findings
• (Suspected) congenital CNS anomalies: at admission, thereafter depend-
ing on clinical condition and CUS findings

 ppendix 5.2: How to Distinguish Physiological

A
from Pathological Echodensities in the White Matter

PVE are likely physiological (see Figs. 4.4a–d, 5.6a, b) if the echogenicity is
[1, 3]:

• Less than the echogenicity of the choroid plexus and:

–– Homogeneous
–– Bilateral
–– Symmetrical (shape and location)
–– Linear
–– Of short duration (< 7 days) and fading before TEA

PVE are more likely to be non-physiological (see Figs. 4.4e–j, 5.3c, d,

5.5c, d, 5.6c, d and 5.7a–c) and probably indicating white matter injury if
the echogenicity:
• Is equal to or exceeds that of the choroid plexus
• Extends into the deep white matter
136 5 Timing of Ultrasound Examinations

• Is inhomogeneous
• Is patchy
• Is asymmetrical
• Is of longer duration (≥ 7 days)
• Persists beyond TEA

Physiological PVE Non-physiological PVE

Echogenicity < plexus Echogenicity ≥ plexus
Homogeneous Inhomogeneous
Symmetrical (shape, location) Less symmetrical
Linear Patchy
Well defined Less defined
Short duration and < TEA ≥ 7 days and/or ≥ TEA

References

1. Leijser LM et al (2009) Frequently encountered cranial ultrasound features in the white

matter of preterm infants: correlation with MRI. Eur J Paediatr Neurol 13:317–326
2. van Wezel-Meijler G et al (2011) Diffuse Hyperechogenicity of Basal Ganglia and
Thalami in Preterm Neonates: A Physiologic Finding? Radiology 258:944–950
3. Boxma A et al (2005) Sonographic detection of the optic radiation. Acta Paediatr
94:1455–1461

Further Reading

Benders MJ et al (2014) Neuroimaging of white matter injury, intraventricular and cer-

ebellar hemorrhage. Clin Perinatol 41:69–82
Bracci R et al (2006) The timing of neonatal brain damage. Biol Neonate 90:145–155
Brouwer AJ et al (2013) Treatment of neonatal progressive ventricular dilatation: a single-­
center experience. J Matern Fetal Neonatal Med 28 S1: 2273–2279
Brouwer AJ et al (2014) Early and late complications of germinal matrix-intraventricular
haemorrhage in the preterm infant: what is new? Neonatology 106:296–303
Daneman A et al (2006) Imaging of the brain in full-term neonates: does sonography still
play a role? Pediatr Radiol 36:636–646
Ecury-Goossen GM et al (2010) The clinical presentation of preterm cerebellar haemor-
rhage. Eur J Pediatr 169:1249–1253
Further Reading 137

Edwards AD et al (2018) Effect of MRI on preterm infants and their families: a random-
ized trial with nested diagnostic and economic evaluation. Arch Dis Child Fetal
Neonatal Ed 103(1):F15–F21
Epelman M et al (2012) Head ultrasound and MR imaging in the evaluation of neona-
tal encephalopathy: competitive or complementary imaging studies? Magn Reson
Imaging Clin N Am 20:93–115
Fumagalli M et al (2015) From germinal matrix to cerebellar hemorrhage. J Matern Fetal
Neonatal Med 28(Suppl 1):2280–2285
Hagmann et al (2010) Cranial ultrasound findings in well newborn Ugandan infants.
Arch Dis Child Fetal NeonatEd 95:F338–F344
Hintz SR et al (2015) Neuroimaging and neurodevelopmental outcome in extremely pre-
term infants. Pediatrics 135:e32–e42
Horsch S et al (2005) Ultrasound diagnosis of brain atrophy is related to neurodevelop-
mental outcome in preterm infants. Acta Paediatr 94:1815–1821
Inder TE et al (2017) Preterm intraventricular hemorrhage/posthemorrhagic hydroceph-
alus. In: Volpe’s neurology of the newborn, 6th edn. Elsevier
Leijser LM et al (2006) Using cerebral ultrasound effectively in the newborn infant. Early
Hum Dev 82:827–835
Leijser LM et al (2007) Cranial ultrasound in metabolic disorders presenting in the neona-
tal period: characteristic features and comparison with MRI. AJNR Am J Neuroradiol
28:1223–1231
Leijser LM et al (2009) Brain imaging findings in very preterm infants throughout the
neonatal period: part I. Incidences and evolution of lesions, comparison between
ultrasound and MRI. Early Hum Dev 85:101–109
Leijser LM et al (2010) Is sequential cranial ultrasound reliable for detection of white mat-
ter injury in very preterm infants? Neuroradiology 52:397–406
Leijser LM et al (2018) Post-hemorrhagic ventricular dilatation in preterm infants: when
best to intervene? Neurology 90(8):e698–e706
Limperopoulos C et al (2017) Cerebellar hemorrhage. In: Volpe’s neurology of the new-
born, 6th edn. Elsevier
McCarthy LK et al (2011) Ultrasonically detectable cerebellar haemorrhage in preterm
infants. Arch Dis Child Fetal Neonatal Ed 96:F281–F285
Meijler G et al (2016). Neonatal cranial ultrasonography. In: Beek, van Rij (eds) Diagnostic
pediatric ultrasound, chapter 3. Thieme
Miller SP et al (2003) Comparing the diagnosis of white matter injury in premature new-
borns with serial MR imaging and transfontanel ultrasonography findings. AJNR Am
J Neuroradiol 24:1661–1669
Neil JJ, Volpe JJ (2017) Encephalopathy of prematurity: clinical-neurological features,
diagnosis, imaging, prognosis, therapy. In: Volpe’s neurology of the newborn, 6th edn.
Elsevier
138 5 Timing of Ultrasound Examinations

Plaisier A et al (2015) Serial cranial ultrasonography or early MRI for detecting preterm
brain injury? Arch Dis Child Fetal Neonatal Ed 100:F293–F300
Sarkar S et al (2018) Outcome of preterm infants with transient cystic periventricular
leukomalacia on serial cranial imaging up to term equivalent age. J Pediatr 195:59.
e3–65.e3
Sie LTL et al (2000) Early MR features of hypoxic-ischemic brain injury in neonates with
periventricular densities on sonogram. Am J Neuroradiol 21:852–861
Skiöld B et al (2019) A novel scoring system for term-equivalent-age cranial ultrasound in
extremely preterm infants. Ultrasound Med Biol 45:786–794
Steggerda SJ et al (2009) Cerebellar injury in preterm infants: incidence and findings on
US and MR images. Radiology 252:190–199
Steggerda SJ et al (2012) Ultrasound detection of posterior fossa abnormalities in full-­
term neonates. Early Hum Dev 88:233–239
Stolwijk LJ et al (2017) Neonatal surgery for noncardiac congenital anomalies: neonates at
risk of brain injury. J Pediatr 182:335–341
Verboon-Maciolek MA et al (2012) Development of cystic periventricular leukomalacia
in newborn infants after rotavirus infection. J Pediatr 160:165–168
Volpe JJ (1989) Intraventricular hemorrhage in the premature infant—current concepts.
Part II. Ann Neurol 25:109–116
de Vries LS et al (1992) The spectrum of leukomalacia using cranial ultrasound. Behav
Brain Res 49:1–6
de Vries LS et al (2004) Ultrasound abnormalities preceding cerebral palsy in high-risk
preterm infants. J Pediatr 144:815–820
de Vries LS et al (2006) The role of cranial ultrasound and magnetic resonance imaging in
the diagnosis of infections of the central nervous system. Early Hum Dev 82:819–825
de Vries LS et al (2015) Progress in neonatal neurology with a focus on neuroimaging in
the preterm infant. Neuropediatrics 4:234–241
de Vries LS et al (2013) Imaging the premature brain: ultrasound or MRI? Neuroradiology
55:S13–S22
de Vries LS, Volpe JJ (2017a) Viral, protozoan and related intracranial infections. In:
Volpe’s neurology of the newborn, 6th edn. Elsevier
de Vries LS, Volpe JJ (2017b) Bacterial and fungal intracranial infections. In: Volpe’s neu-
rology of the newborn, 6th edn. Elsevier
van Wezel-Meijler G et al (2011) Ultrasound detection of white matter injury in very pre-
term neonates: practical implications. Radiology 261:899–906
van Wezel-Meijler G, De Vries LS (2014) Cranial ultrasound-optimizing utility in the
NICU. Curr Pediatr Rev 10:16–27
 6 Scoring Systems

6.1 S
 coring Systems

In order to obtain insight into the severity of lesions and for better prognos-
tication, it is recommended to apply a scoring system for GMH-IVH, CBH,
PVE and PVL. These scoring systems are presented in Appendices 6.1, 6.2
and 6.3, respectively.

Appendix 6.1: Classification of GMH-IVH

Germinal Matrix hemorrhage

Adapted from Volpe [1]:

• Grade 1: GMH with no or minimal IVH (Fig. 6.1)
• Grade 2: IVH (10–50% of the ventricular area on parasagittal view)
(Fig. 6.2)
• Grade 3: IVH (>50% of the ventricular area on parasagittal view); ­usually
with acute dilatation of the lateral ventricle (Fig. 6.3)
• Separate notation: PHVD (Fig. 6.4; see also Figs. 4.6e–g and 4.7)
Posthemorrhagic ventricular dilatation
• Separate notation: concomitant intraparenchymal echodensity (includ-
ing location and extent), representing PVHI, also called venous infarc-
tion* (Figs. 6.5, 6.6, and 6.7; see also Fig. 4.9)

*This unilateral or strikingly asymmetrical echodensity, which is associ-

ated with an ipsilateral IVH, often evolves into a unilateral porencephalic
cyst and/or several smaller cysts over a period of 1–3 weeks (see Figs. 5.11
and 6.7). These smaller cysts should not be confused with c-PVL, which is
generally bilateral and more symmetrical (see Fig. 5.3).

© Springer Nature Switzerland AG 2019 139

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
140 6 Scoring Systems

Fig. 6.1 IVH grade 1. Very preterm infant. (a) Coronal view through the bodies of the
lateral ventricles and (b) parasagittal view through the left lateral ventricle showing an
obvious GMH on the left side (arrow). There also appears to be a smaller GMH on the
right side (green arrow in a)
Appendix 6.1: Classification of GMH-IVH 141

Fig. 6.2 IVH grade 2. Very preterm baby (GA 25+2 weeks), who developed an IVH
immediately after birth. CUS on day 4. (a) Coronal view (the image is somewhat asym-
metrical), showing the right-­sided IVH (arrow); there is a small GMH on the left side
(green arrow); the 3rd ventricle is wide and echogenic (arrowhead), indicating haemor-
rhage; and there seems to be haemorrhage in the right temporal horn (red arrow). (b)
Parasagittal view through the right lateral ventricle showing the IVH (arrow) filling less
than 50% of the lateral ­ventricle. There is a clot in the occipital horn (asterisk), and the
haemorrhage in the temporal horn is also visible (red arrow)
142 6 Scoring Systems

Fig. 6.3 IVH grade 3. Preterm baby: GA 31 weeks, emergency caesarean section
because of placental abruption with severe foetal distress, postnatal transport to the
NICU. The baby initially had a small GMH. (a, b) CUS on 3rd postnatal day (a coronal
view through the body of the lateral ventricles and b parasagittal view through the left
lateral ventricle) shows a large left-sided IVH (filling > 50% of the ventricle). (c–e) Two
days later, CUS shows extension of the IVH: there is now also an IVH on the right side,
while the left-sided IVH is now almost completely filling the lateral ventricle and
causes acute distention of the lateral ventricle (e). Note the haemorrhage in the tem-
poral (arrows) and occipital (green arrow) horns
Appendix 6.1: Classification of GMH-IVH 143

Fig. 6.3 (continued)

144 6 Scoring Systems

Fig. 6.3 (continued)

Appendix 6.1: Classification of GMH-IVH 145

Fig. 6.4 PHVD in a very preterm neonate (GA 27+4 weeks) who developed an IVH
grade 3 on the first postnatal day. Same infant as in Fig. 4.6e–g, 9 days later. CUS at
postnatal age of 17 days (a coronal view through the frontal horns of the lateral ven-
tricles, b midsagittal view, c parasagittal view through the right lateral ventricle) shows
dilatation of the lateral ventricles and third ventricle (arrow in b), remnants of the bleed
(green arrows in c) and echogenicity of the ventricular walls (arrowheads in a and c).
Thanks to treatment with repetitive lumbar punctures to prevent increased intracra-
nial pressure, the ventricular dilatation has improved as compared to previous images
(see also Fig. 4.6e–g)
146 6 Scoring Systems

Fig. 6.4 (continued)

Appendix 6.1: Classification of GMH-IVH 147

Fig. 6.5 IVH with PVHI. Very preterm neonate, GA 26 weeks (same infant as in
Fig. 5.11). (a, b) CUS scan on the 3rd postnatal day shows large right-sided IVH and an
intraparenchymal echodensity, representing PVHI (arrows). (a) Coronal view at the
level of the frontal horns of the lateral ventricles, showing the IVH and the PVHI, adja-
cent to the frontal horn of the lateral ventricle. (b) Parasagittal view, showing the PVHI
in the right fronto-parietal area. See Fig. 5.11: same infant, scanned at PMA 37 weeks.
CUS shows cystic degeneration of the PVHI (large porencephalic cyst and multiple
smaller cysts)
148 6 Scoring Systems

Fig. 6.6 IVH with PVHI. CUS in a very preterm neonate with intrauterine growth restric-
tion (GA 26+1 weeks). On the first postnatal day, CUS shows a large left-sided IVH and an
intraparenchymal echodensity, representing PVHI. (a) Coronal view at the level of the
frontal horns of the lateral ventricles, showing the large IVH, causing a midline shift and
PVHI. (b) Left parasagittal view showing the very large PVHI extending into the frontal,
parietal and temporal lobes
Appendix 6.1: Classification of GMH-IVH 149

Fig. 6.7 IVH with small PVHI. Preterm infant, GA 31 weeks, complicated pregnancy.
Emergency caesarean section with ventouse delivery of the head. CUS on first postna-
tal day already showed IVH with PVHI. (a–c) CUS on second postnatal day (a coronal
through body of the lateral ventricles, b parasagittal through right lateral ventricle and
c parasagittal through right insular area) shows right-sided IVH grade 2 (green arrows)
and an ipsilateral echogenic parenchymal lesion (arrows), representing a small venous
infarction (PVHI). (d, e) CUS 2 weeks later, before discharge to a level II hospital, shows
the venous infarction, now undergoing cystic degeneration (arrows). (f–h) TEA MRI. (f)
T2-weighted transverse image at supraventricular level shows a porencephalic cyst in
the right parietal area. (g) T1-weighted transverse image at basal ganglia level shows
somewhat asymmetrical myelination of the posterior limb of the internal capsule
(PLIC) and a small interruption within the PLIC on the right side (red arrow). (h) Diffusion
tractography shows asymmetry of the PLIC: the right-sided PLIC being less well devel-
oped. This asymmetrical development of the PLIC results from the venous infarction
and may be of clinical significance. The outcome of this baby is yet unknown
150 6 Scoring Systems

Fig. 6.7 (continued)

Appendix 6.1: Classification of GMH-IVH 151

Fig. 6.7 (continued)

152 6 Scoring Systems

Fig. 6.7 (continued)

f

g
Appendix 6.2: Classification of CBH 153

Fig. 6.7 (continued)

In the past, PVHI was also named grade 4 IVH. We prefer not to use this
term as it suggests primary haemorrhage, while PVHI represents a haemor-
rhagic, venous infarction.

Appendix 6.2: Classification of CBH

Adapted from Steggerda et al. [2] and Parodi et al. [3]:

• Grade 0: normal echogenicity of the cerebellar vermis and hemispheres

with normal anatomic features. No signs of focal destruction or atrophy
(Fig. 6.8; see also Figs. 3.19 and 3.20)
154 6 Scoring Systems

Fig. 6.8 No CBH. CUS in full-term infant, using the left mastoid fontanelle as acoustic
window. (a) Slightly oblique, high transverse or axial view, showing normal cerebellar
parenchyma with normal echogenic fissures extending from one hemisphere to the
other. (b) Oblique, lower transverse view through the cerebellum, 4th ventricle (green
asterisk) and pons (blue asterisk). The cerebellar vermis (arrow) is generally somewhat
more echogenic than the hemispheres (green arrow). (c) Oblique coronal view through
the cisterna magna (red arrow), foramen of Magendie (blue asterisk), vermis (blue
arrow), hemispheres (green arrow) and 4th ventricle (green asterisk). Showing normal
cerebellar parenchyma with numerous foliae and the vermis being somewhat more
echogenic than the hemispheres. Note that the right hemisphere, being furthest away
from the transducer, is more vaguely depicted than the left hemisphere
Appendix 6.2: Classification of CBH 155

Fig. 6.8 (continued)

• Grade 1: small (≤4 mm) (focal) punctate lesion(s) in the cerebellar

parenchyma [4].
Of note, these punctate lesions are usually difficult to detect on CUS
(Fig. 6.9; see also Fig. 5.8) but are a frequent finding on MRI performed
in preterm infants. There is generally no atrophy on follow-up ultra-
sound or MRI.
• Grade 2: limited CBH, well detectable with CUS, larger than a punctate
lesion (>4 mm) but involving at the most 1/3 of the cerebellar hemisphere.
Usually these lesions involve the lateral or inferior convexity of the
cerebellar hemisphere. On follow-up ultrasound, focal cystic degenera-
tion or atrophy may be seen, involving at the most 1/3 of the cerebellar
hemisphere (Fig. 6.10).
• Grade 3: extensive CBH, involving more than 1/3 of the cerebellar hemi-
sphere (Fig. 6.11), often leading to destruction or atrophy of the cerebel-
lar hemisphere on follow-up CUS (Fig. 6.12).
• A separate notation is added for sidedness, uni- or bilateral occurrence
and for lesions also (or only) involving the cerebellar vermis.
156 6 Scoring Systems

Fig. 6.9 CBH grade 1. Full-term infant with perinatal asphyxia, treated with therapeu-
tic hypothermia. (a) CUS at 4th postnatal day using the right mastoid fontanelle (trans-
verse or axial view) shows small areas of increased echogenicity in right cerebellar
hemisphere (arrows) suspect for small haemorrhages. (b, c) T2-weighted (b) and
susceptibility-­weighted (c) MR images on the 7th postnatal day confirm two punctate
(grade 1) cerebellar haemorrhages (arrows in b) in the right hemisphere. Note the
enhancement of the small bleeds on the susceptibility-weighted scan, due to so-­
called blooming artefact. This effect improves the detection of small haemorrhages
Appendix 6.2: Classification of CBH 157

Fig. 6.9 (continued)

b

c
158 6 Scoring Systems

Fig. 6.10 CBH grade 2. Very preterm neonate, GA 25+2 weeks, who developed an IVH
grade 1 on the first postnatal day. Two days later, a CBH was diagnosed. (a) Coronal and
(b) parasagittal CUS through the anterior fontanelle shows an echogenic lesion in the
right cerebellar hemisphere (arrows). (c) Axial CUS through the left mastoid fontanelle
confirms the presence of CBH grade 2 (involving < 1/3 of cerebellar parenchyma) at
the convexity of the right cerebellar hemisphere (arrow). (d) Three weeks later, axial
CUS through the right mastoid fontanelle shows beginning cystic degeneration of the
lesion (arrow). (e) T2-weighted axial MRI scan at TEA shows remnants of the bleed
(arrow) and clearly demonstrates that the right cerebellar hemisphere is now smaller
than the left with partial loss of the normal anatomic features
Appendix 6.2: Classification of CBH 159

Fig. 6.10 (continued)

160 6 Scoring Systems

Fig. 6.10 (continued) e

Appendix 6.2: Classification of CBH 161

Fig. 6.11 CBH grade 3. Coronal (a), midsagittal (b) and parasagittal through the left
lateral ventricle (c) ultrasound scans using the anterior fontanelle as acoustic window
and axial or transvers (d) and coronal (e) scans through, respectively, the left and the
right mastoid fontanelle in a very preterm and growth-retarded neonate (GA 28+5
weeks, birth weight 840 gram, scan performed on the 9th postnatal day). The baby was
initially stable but developed a Gram-negative sepsis with respiratory and circulatory
failure and thrombocytopenia on the 8th postnatal day. The scans through the ante-
rior fontanelle show irregular enlargement of the posterior fossa with loss of the nor-
mal anatomical cerebellar features and increased echogenicity (arrows). The lateral
ventricles and the 3rd ventricle (asterisk) are dilated due to outflow obstruction of the
fourth ventricle. Also note that the vermis is not well delineated on the midsagittal
image. The scans through the mastoid fontanelle confirm extensive haemorrhage
within (arrows) and around (green arrow) the cerebellum. The baby died the next day
due to severe vital instability related to the massive posterior fossa haemorrhage
162 6 Scoring Systems

Fig. 6.11 (continued)

Appendix 6.2: Classification of CBH 163

Fig. 6.11 (continued)

164 6 Scoring Systems

Fig. 6.12 Coronal CUS through the right mastoid fontanelle (first postnatal day) (same
infant as Fig. 6.6). The left cerebellar hemisphere (arrow) is dysplastic, and the vermis
(asterisk) has largely vanished due to compression (obstructed 4th ventricular outflow,
resulting from the massive supratentorial IVH), combined with haemorrhage in the 4th
ventricle and antenatal CBH). The 4th ventricle (arrowhead) is severely dilated. Also
showing the large intraparenchymal echodensity, representing PVHI in the left cere-
bral hemisphere and the dilated right lateral ventricle

Appendix 6.3: Classification of PVE

Periventricular echogenicities

Adapted from van Wezel-Meijler et al. [5]:

• Grade 0: normal echogenicity of the periventricular white matter (the

echogenicity of the periventricular white matter being less than that of
the choroid plexus) (Fig. 6.13; see also Figs. 4.4a–d and 5.6a, b)
• Grade 1: mildly abnormal echogenicity of the periventricular white mat-
ter, mainly homogeneous, but with the affected region (or smaller areas
within the affected region) being almost as bright or as bright as the cho-
roid plexus (Fig. 6.14; see also Fig. 5.5a, b)
• Grade 2: seriously abnormal echogenicity of the periventricular white mat-
ter, the affected region (or smaller areas within the affected region) being
brighter than the choroid plexus and/or the affected region being inhomo-
geneous (Figs. 6.15, 6.16, and 6.17; see also Figs. 5.3c, d, 5.5c, d and 5.6c, d)
Appendix 6.3: Classification of PVE 165

Fig. 6.13 PVE grade 0. (a, b) CUS on the second postnatal day in very preterm neonate,
GA 25+3 weeks, showing normal echogenicity of the periventricular white matter,
being subtle, homogeneous and less echogenic than the choroid plexus. (a) Coronal
view at the level of the trigone of the lateral ventricles. (b) Parasagittal view through
the left insula. Note the symmetrical linear echogenicity, running parallel to the tri-
gone of the lateral ventricles (arrow in a), being a normal phenomenon. (c, d) Coronal
and parasagittal CUS on the second postnatal day in uncomplicated preterm neonate,
GA 31 weeks, shows subtle, homogeneous echogenicity of the periventricular white
matter, less echogenic than the choroid plexus (plexus not shown)
166 6 Scoring Systems

Fig. 6.13 (continued)

Appendix 6.3: Classification of PVE 167

Fig. 6.14 PVE grade 1. Preterm neonate, GA 28+3 weeks, IRDS, lung hypoplasia and
artificial ventilation. The first CUS scan performed a few hours after birth was normal.
CUS on the second postnatal day (a) coronal at the level of the trigone of the lateral
ventricles and (b) parasagittal through the left insular area. The periventricular white
matter is somewhat inhomogeneous and moderately echogenic, the echogenicity
being almost equal to that of the choroid plexus (red asterisk). The PVE lasted more
than 7 days and gradually improved afterwards (PVE grade 1 and PVL grade 1). Also
note that (a) the normal echogenicity running parallel to the trigone of the lateral ven-
tricles is not well distinguishable (see Fig. 6.13a). (c, d) Around TEA the PVE is no longer
present, but the subarachnoidal space is wide (asterisks), and the lateral ventricle has a
somewhat irregular shape, indicating white matter volume loss
168 6 Scoring Systems

Fig. 6.14 (continued)

Appendix 6.4: Classification of PVL 169

Fig. 6.14 (continued)

Appendix 6.4: Classification of PVL

Adapted from de Vries et al. [6]:

• Grade 1: transient abnormal PVE persisting for ≥7 days but without cys-
tic evolution (see Figs. 5.6 c, d and 6.14)
• Grade 2: transient abnormal PVE evolving into small, localised fronto-­
parietal cysts (Fig. 6.18; see also Figs. 5.5 and 6.15)
• Grade 3: abnormal PVE evolving into extensive periventricular cystic
lesions (see Fig. 5.3)
• Grade 4: densities extending into the deep white matter evolving into
extensive cystic lesions (Fig. 6.19)

The incidence of “classic” cystic PVL (c-PVL) where this classification

refers to has fortunately declined over the last decades. Grade 3 and 4 PVL
are nowadays rare and there has been a shift from c-PVL towards a more
subtle, non-cystic form of white matter injury (so-called diffuse or subtle
white matter injury) which is less well detected with CUS.
170 6 Scoring Systems

Fig. 6.15 PVE grade 2 evolving into PVL grade 2. Preterm neonate, GA 31 weeks, E. coli
sepsis with respiratory and circulatory failure. (a) Coronal view through the trigone of
the lateral ventricles and (b) parasagittal view through the left insular region. CUS on
postnatal day 10, showing increased echogenicity of the periventricular white matter,
the echogenicity being inhomogeneous and patchy and equal to that of the choroid
plexus (PVE grade 2). (c, d) Respectively, coronal through parieto-occipital lobes and
parasagittal through left lateral ventricle CUS 1 week later at a PMA of 33+3 weeks, still
showing the inhomogeneous PVE and now also showing a small cyst in the left pari-
etal area (arrow). The lateral ventricle has an irregular shape, due to white matter vol-
ume loss. (e, f) MRI performed at a PMA of 34+2 weeks. T1-weighted (e) and T2-weighted
(f) images at high ventricular level, showing multiple punctate white matter lesions
(PWML) and some small cystic lesions (arrow)
Appendix 6.4: Classification of PVL 171

Fig. 6.15 (continued)

172 6 Scoring Systems

Fig. 6.15 (continued)

Appendix 6.4: Classification of PVL 173

Fig. 6.15 (continued)

e

f
174 6 Scoring Systems

Fig. 6.16 PVE grade 2. Preterm neonate, GA 30 weeks. Born anaemic, after emergency
caesarean section because of placenta praevia and blood loss. CUS on 4th postnatal
day. (a) Coronal through trigone of the lateral ventricles, (b) coronal through parieto-­
occipital lobe and (c) parasagittal through left insular area showing inhomogeneously,
patchy and asymmetrically increased echogenicity, being as echogenic as the choroid
plexus. (d) Transverse T-weighted MR image at TEA shows clusters of punctate white
matter lesions
Appendix 6.4: Classification of PVL 175

Fig. 6.16 (continued)

176 6 Scoring Systems

Fig. 6.17 PVE grade 2. Preterm neonate, GA 31+2 weeks, born as second twin, IRDS
(same infant as Fig. 4.4i, j). On the 2nd postnatal day, the (a) coronal at the level of the
parieto-occipital lobes and (b) parasagittal through the right lateral ventricle CUS
show seriously and inhomogeneously increased echogenicity of the periventricular
white matter, much brighter than the choroid plexus (PVE grade 2). The baby died due
to severe apnoeic spells after redirection of intensive care
Appendix 6.4: Classification of PVL 177

Fig. 6.18 PVL grade 2. Preterm infant born at 28 weeks’ gestation after emergency
caesarean section because of foetal distress. (a, b) CUS on first postnatal day shows
inhomogeneously increased, patchy echogenicity in the parietal area, mainly on the
right side. (c–e) One month later, bilateral small cystic lesions are seen in the periven-
tricular white matter. (c) Coronal through trigone of the lateral ventricles. (d, e)
Parasagittal through, respectively, right and left insular area
178 6 Scoring Systems

Fig. 6.18 (continued)

Appendix 6.4: Classification of PVL 179

Fig. 6.18 (continued)

180 6 Scoring Systems

Fig. 6.19 PVL grade 4. Preterm infant born at 29 weeks’ gestation. Monochorionic twin
pregnancy, complicated by twin-to-twin transfusion syndrome and intrauterine foetal
demise of the co-twin (donor). Afterwards deterioration of the condition of the surviv-
ing twin (recipient) needing an emergency caesarean section. CUS 2–3 weeks postna-
tally shows extensive cystic lesions extending into the deep white matter. The baby
died after redirection of intensive care (courtesy professor Linda de Vries, Wilhelmina
Children’s Hospital, Utrecht)
References 181

Fig. 6.19 (continued)

References
1. Volpe JJ (1989) Intraventricular hemorrhage in the premature infant—current con-
cepts. Part II. Ann Neurol 25:109–116
2. Steggerda SJ et al (2009) Cerebellar injury in preterm infants: incidence and findings
on US and MR images. Radiology 252:190–199
3. Parodi A et al (2015) Accuracy of ultrasound in assessing cerebellar haemorrhages in
very low birthweight babies. Arch Dis Child Fetal Neonatal Ed 100(4):F289–F292
4. Steggerda SJ, van Wezel-Meijler G (2016) Cranial ultrasound of the immature cerebel-
lum: role and limitations. Semin Fetal Neonatal Med 21:295–304
5. van Wezel-Meijler G et al (1998) Magnetic resonance imaging of the brain in prema-
ture infants during the neonatal period. Normal phenomena and reflection of mild
ultrasound abnormalities. Neuropediatrics 29:89–96
6. de Vries LS et al (1992) The spectrum of leukomalacia using cranial ultrasound. Behav
Brain Res 49:1–6
182 6 Scoring Systems

Further Reading

Benders MJ et al (2014) Neuroimaging of white matter injury, intraventricular and cer-

ebellar hemorrhage. Clin Perinatol 41:69–82
Cowan FM, De Vries LS (2005) The internal capsule in neonatal imaging. Semin Fetal
Neonatal Med 10:461–474
de Vries LS et al (1999) Asymmetrical myelination of the posterior limb of the internal
capsule in infants with periventricular haemorrhagic infarction: an early predictor of
hemiplegia. Neuropediatrics 30:314–319
de Vries LS et al (2015) Progress in neonatal neurology with a focus on neuroimaging in
the preterm infant. Neuropediatrics 4:234–241
Groenendaal F et al (2010) Complications affecting preterm neonates from 1991 to 2006:
what have we gained? Acta Paediatr 99:354–358
Hamrick SE et al (2004) Trends in severe brain injury and neurodevelopmental out-
come in premature newborn infants: the role of cystic periventricular leukomalacia. J
Pediatr 145:593–599
Inder TE et al (2017) Preterm intraventricular hemorrhage/posthemorrhagic hydroceph-
alus. In: Volpe JJ (ed) Volpe’s neurology of the newborn, 6th edn. Elsevier, Philadelphia
Leijser LM et al (2008) Comparing brain white matter on sequential cranial ultrasound
and MRI in very preterm infants. Neuroradiology 50:799–811
Leijser LM et al (2010) Is sequential cranial ultrasound reliable for detection of white mat-
ter injury in very preterm infants? Neuroradiology 52:397–406
Limperopoulos C et al (2017) Cerebellar hemorrhage. In: Volpe JJ (ed) Volpe’s neurology
of the newborn, 6th edn. Elsevier, Philadelphia
Miller SP et al (2003) Comparing the diagnosis of white matter injury in premature new-
borns with serial MR imaging and transfontanel ultrasonography findings. AJNR Am
J Neuroradiol 24:1661–1669
Neil JJ, Volpe JJ (2017) Encephalopathy of prematurity: clinical-neurological features,
diagnosis, imaging, prognosis, therapy. In: Volpe JJ (ed) Volpe’s neurology of the new-
born, 6th edn. Elsevier, Philadelphia
Steggerda SJ et al (2013) Small cerebellar hemorrhage in preterm infants: perinatal and
postnatal factors and outcome. Cerebellum 12(6):794–801
van Wezel-Meijler G, de Vries LS (2014) Cranial ultrasound-optimizing utility in the
NICU. Curr Pediatr Rev 10:16–27
 7 Limitations of Cranial Ultrasonography
and Recommendations for MRI

7.1 L
 imitations of Cranial Ultrasonography

The advantages of CUS are numerous and widely appreciated (see Chap. 1).
It is however important to acknowledge the limitations of CUS:

• Image quality can be affected by small acoustic windows, thick hair or hats
used for ventilatory support systems. Although the adaptation of trans-
ducer frequency in individual situations (see Chap. 2) and the application
of additional acoustic windows (see Chap. 3) enhance the possibilities of
CUS, some structures and abnormalities remain difficult to visualise.
• The brain’s convexity is not well visualised: (small) arterial cortical
infarctions and watershed lesions may be overlooked, especially in the
first days after the event; subtle aspects of cortical folding will not be reli-
ably assessed, and extracerebral haemorrhage located at the convexity of
the cerebral hemispheres (i.e. subdural, epidural and subarachnoidal
haemorrhages) may remain beyond the scope of CUS.
• Hypoglycaemic parenchymal injury, often involving the occipital areas,
may not be recognised. Using the posterior fontanelle as the acoustic win-
dow may contribute to detect occipital parenchymal injury (see Chap. 3).
• Some lesions resulting from infection, such as (micro) abscesses and
encephalitis, may not be optimally recognised by CUS.
• CBH and other abnormalities of the cerebellum may have important
consequences for neurodevelopment. These and other posterior fossa
abnormalities are usually detected, especially if a­ dditional scanning is
performed through the mastoid and posterior fontanelles. It is, however,

© Springer Nature Switzerland AG 2019 183

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
184 7 Limitations of Cranial Ultrasonography and Recommendations…

not always possible to define abnormalities precisely and to determine

the exact location and extent of abnormalities (see Chaps. 3 and 6).
• Myelination is not visualised. Involvement in lesions of the internal
capsule and other white matter tracts, which may be of major impor-
tance for neurological outcome, cannot be determined with certainty by
CUS.
• Injury to the basal ganglia in hypoxic-ischaemic encephalopathy and
areas of focal infarction are usually detected, but they may not be defined
well enough for accurate prognostication.
• Diffuse white matter injury and punctate CBH, frequently occurring in
very preterm infants, are not reliably detected by CUS (see Chap. 6).

7.2 R
 ole of MRI

In modern neonatology, CUS and MRI are complementary neuroimaging tools.

Although MRI cannot replace serial CUS, many conditions require MRI for
proper diagnosis and treatment, while in others, MRI contributes to diag-
nosis and prognostication.
MRI depicts brain maturation, including myelination, in detail. It helps
to define the timing of pathological processes and enables prognostication
in many cases. It establishes the precise site, origin and extent of lesions.
Depending on location and size, MRI may detect lesions that CUS does not.
It allows for detection of diffuse and non-cystic white matter injury and
punctate CBH frequently occurring in very preterm infants. Diffusion-
weighted MR imaging allows early detection of hypoxic-­ischaemic brain
injury, and with magnetic resonance venography and arteriography, the
cerebral veins and arteries can be assessed. Diffusivity measurements enable
quantification of maturation and injury, while volume measurements enable
quantification of brain growth and tissue loss.
However, MRI does not allow for frequent, serial imaging, and early
imaging within the first few days after birth is hard to realise, especially in
unstable neonates.
In addition, although safe when necessary precautions are taken and
guidelines are precisely followed, MRI is more burdening than CUS for the
sick and/or preterm neonate.
7.2 Role of MRI 185

Some conditions, such as calcifications, germinolytic cysts, subependy-

mal pseudocysts (Fig. 7.1) and LSV (Fig. 7.2; see also Fig. 4.5i, j), are better
or only depicted by ultrasound.

Fig. 7.1 (a–c) CUS performed around TEA in preterm neonate (GA 33+5 weeks, uncom-
plicated pregnancy and delivery). (a) coronal through body of the lateral ventricles, (b)
parasagittal through right lateral ventricle
186 7 Limitations of Cranial Ultrasonography and Recommendations…

Fig. 7.1 (c) parasagittal just left of the midline, showing a germinolytic cyst on the
right side (arrows) and a smaller one on the left side (green arrows). (d, e) TEA MRI per-
formed on the same day. (d) Axial T1-weighted image at midventricular level, showing
normal anatomy and maturation and no abnormalities. Note the nice symmetrical
myelination of the PLIC (asterisk) (compare with Fig. 6.7i–k). There are some movement
artefacts. (e) coronal T2-weighted MR image. While the germinolytic cysts are obvious
on the CUS images, they are hardly discernible on MRI (arrow)
7.2 Role of MRI 187

Fig. 7.1 (continued)

d

e
188 7 Limitations of Cranial Ultrasonography and Recommendations…

Fig. 7.2 Preterm neonate, GA 30+2 weeks, monochorionic twin pregnancy, twin-to-­
twin transfusion syndrome. (a–c) CUS (a coronal through the frontal horns of the lat-
eral ventricles, b parasagittal through the right insular area, c parasagittal through the
left lateral ventricle) shows obvious bilateral echogenicity of the lenticulostriate ves-
sels (arrows), so-called LSV. Also showing inhomogeneous PVE grade 1
7.2 Role of MRI 189

Fig. 7.2 (continued) (d, e) MRI at TEA (PMA 38 weeks). T1-weighted (d), respectively,
T2-weighted (e) transverse images at midventricular level. The LSV is not depicted:
there is no MR equivalent for LSV. Note the normal high signal intensity of myelin in
the PLIC (asterisk) on the T1-weighted image. As this infant was 2 weeks younger at
scanning (PMA 38 weeks), this normal high signal is less obvious than in Fig. 7.1d. The
asymmetrical appearance of the MR images is due to the asymmetrical position of the
infant in the coil
190 7 Limitations of Cranial Ultrasonography and Recommendations…

Fig. 7.2 (continued)

d

e
7.2 Role of MRI 191

Routine MRI around TEA in ex-preterm infants is useful for precise and
reliable detection of (small) lesions but may not add significantly to the pre-
dictive value of high-quality CUS and may be a burden to the child and its
parents. The advantages of TEA MRI in these infants should be carefully
weighed against possible disadvantages, and parents should be well
informed on the considerations.

7.2.1 C
 onditions in Which MRI Contributes to Diagnosis
and/or prognostication

• Very preterm birth (white matter injury, punctate lesions)

• Hypoxic-ischaemic encephalopathy in (near) term neonates
• Seizures and other neurological symptoms
• Arterial infarction
• Supratentorial parenchymal abnormalities diagnosed or suspected by CUS
• Infratentorial abnormalities diagnosed or suspected by CUS
• Congenital or acquired infections of the CNS
• Congenital malformations of the CNS
• Subdural and subarachnoidal haemorrhage
• Symptomatic hypoglycaemia
• Hyperbilirubinaemia needing exchange transfusion
• Metabolic disease with CNS involvement
• PHVD
• Cerebral sinovenous thrombosis
• (Suspected) abnormalities at the brain’s convexity

In the Appendix, indications for MRI are presented. In (near) term neo-
nates with hypoxic-ischaemic encephalopathy, optimal information is
obtained when MRI is performed 4–7 days after the incident. In infants
presenting with acute neurological symptoms, MRI is preferably done ear-
lier to enable timely diagnosis. In very preterm infants, the best timing is
probably around TEA (PMA 40–44 weeks), unless earlier diagnosis is of
importance for further treatment and management.
192 7 Limitations of Cranial Ultrasonography and Recommendations…

7.3 R
 ole of CT

The radiation dose involved in CT scanning is significant, and in most cases, CT

has little or no additional diagnostic value as compared to high-quality CUS
and MRI. Therefore, neonatal cerebral CT should only be applied for some rare
conditions. These include suspected calcifications with inconclusive CUS, acute
subdural or subarachnoidal haemorrhages if intervention is considered and
MRI is not readily available, and skull fractures following (suspected) trauma.

Appendix: Indications for Neonatal MRI Examinations

Adapted from the Dutch National guidelines on neonatal neuroimaging (2015).

• Seizures
• Other neurological symptoms, insufficiently explained by CUS findings
• Symptomatic hypoglycaemia, depending on total duration of hypogly-
caemia and severity of clinical symptoms
• Hyperbilirubinaemia needing exchange transfusion and one or both of
the following:
–– Neurological symptoms
–– CUS abnormalities
• Hypoxic-ischaemic encephalopathy
• IVH with PHVD and/or PVHI
• CNS infection
• (Suspected) congenital CNS abnormalities
• (Suspected) CSVT
• (Suspected) posterior fossa abnormalities
• Parenchymal injury:
–– PVL ≥ grade 2
–– Parenchymal haemorrhage
–– Stroke
–– Consider MRI in PVE grade 2, not resolving within 1 week, depend-
ing on the serial CUS findings (see also Chap. 5)
• Symptomatic intracranial, extracerebral haemorrhage
Further Reading 193

Further Reading

Anderson PJ et al (2015) The predictive validity of neonatal MRI for neurodevelopmental

outcome in very preterm children. Semin Perinatol 2015(39):147–158
Boardman JP et al (2013) Hypoglycaemia and neonatal brain injury. Arch Dis Child Educ
Pract Ed 98:2–6 (review)
Burns CM et al (2008) Patterns of cerebral injury and neurodevelopmental outcomes after
symptomatic neonatal hypoglycemia. Pediatrics 122:65–74
Cheong JLY, Miller SP (2018) Imaging the neonatal brain in the 21st century: why, when,
and how? Arch Dis Child Fetal Neonatal Ed 103:F4–F5
Cowan F et al (2005) Does cranial ultrasound imaging identify arterial cerebral infarction
in term neonates? Arch Dis Child Fetal Neonatal Ed 90:F252–F256
Daneman A et al (2006) Imaging of the brain in full-term neonates: does sonography still
play a role? Pediatr Radiol 36:636–646
Daneman A, Epelman M (2015) Neurosonography: in pursuit of an optimized examina-
tion. Pediatr Radiol 3:S406–S412
Dinan D et al (2014) Easily overlooked sonographic findings in the evaluation of neo-
natal encephalopathy: lessons learned from magnetic resonance imaging. Semin
Ultrasound CT MR 35:627–651
Edwards AD (2018) Effect of MRI on preterm infants and their families: a randomised
trial with nested diagnostic and economic evaluation. Arch Dis Child Fetal Neonatal
Ed 103:F15–F21
Epelman M et al (2010) Neonatal encephalopathy: a prospective comparison of head US
and MRI. Pediatr Radiol 40:1640–1650
Epelman M et al (2012) Head ultrasound and MR imaging in the evaluation of neona-
tal encephalopathy: competitive or complementary imaging studies? Magn Reson
Imaging Clin N Am 20:93–115
Epelman M et al (2015) Differential diagnosis of Intracranial cystic lesions at head US:
correlation with CT and MRI imaging. Radiographics 26:173–196
Groenendaal F, De Vries LS (2017) Fifty years of brain imaging in neonatal encephalopa-
thy following perinatal asphyxia. Pediatr Res 81:150–155
Janvier A, Barrington K (2012) Trying to predict the future of ex-preterm infants: who
benefits from a brain MRI at term? Acta Paediatrica 101:1016–1017
Leijser LM et al (2010) Lenticulostriate vasculopathy in very preterm infants. Arch Dis
Child Fetal Neonatal Ed 95(1):F42–F46
Mathur AM et al (2010) Understanding brain injury and neurodevelopmental disabili-
ties in the preterm infant: the evolving role of advanced magnetic resonance imaging.
Semin Perinatol 34:57–66
Parodi A et al (2015) Accuracy of ultrasound in assessing cerebellar haemorrhages in very
low birthweight babies. Arch Dis Child Fetal Neonatal Ed 100:F289–F292
194 7 Limitations of Cranial Ultrasonography and Recommendations…

Pearce R, Baardsnes J (2012) Term MRI for small preterm babies: do parents really want to
know and why has nobody asked them? Acta Paediatr 101:1013–1015
Plaisier A et al (2015) Serial cranial ultrasonography or early MRI for detecting preterm
brain injury? Arch Dis Child Fetal Neonatal Ed 100:F293–F300
Racine E et al (2017) The ‘ouR-HOPE’ approach for ethics and communication about
neonatal neurological injury. Dev Med Child Neurol 59:125–135
Rademaker KJ et al (1993) Subependymal pseudocysts: ultrasound diagnosis and findings
at follow-up. Acta Paediatr 82:394–399
Raets MM et al (2013) Serial cranial US for detection of cerebral sinovenous thrombosis
in preterm infants. Radiology 269:879–886
Ramenghi LA et al (2009) Neonatal cerebral sinovenous thrombosis. Semin Fetal Neonatal
Med 14:278–283
Rutherford MA et al (2012) Neonatal stroke. Arch Dis Child Fetal Neonatal Ed
97:F377–F384
Skiöld B et al (2012) Neonatal magnetic resonance imaging and outcome at age 30 months
in extremely preterm infants. J Pediatr 160:559–566
Sisman J et al (2018) Lenticluostriate vasculopathy in preterm infants: a new classification,
clinical association and neurodevelopmental outcome. J Perinatol 38:1370–1378
Skiöld B et al (2019) A novel scoring system for term-equivalent-age cranial ultrasound in
extremely preterm infants. Ultrasound Med Biol 45:786–794
Steggerda SJ et al (2009) Cerebellar injury in preterm infants: incidence and findings on
US and MR images. Radiology 252:190–199
de Vries LS et al (1999) Asymmetrical myelination of the posterior limb of the internal
capsule in infants with periventricular haemorrhagic infarction: an early predictor of
hemiplegia. Neuropediatrics 30:314–319
de Vries LS et al (2006) The role of cranial ultrasound and magnetic resonance imaging in
the diagnosis of infections of the central nervous system. Early Hum Dev 82:819–825
de Vries LS, Cowan FM (2007) Should cranial MRI screening of preterm infants become
routine? Nat Clin Pract Neurol 3:532–533
de Vries LS et al (2015) Should early cranial MRI of preterm infants become routine? Arch
Dis Child Fetal Neonatal Ed 100:F284–F285
van Wezel-Meijler G et al (2011) Ultrasound detection of white matter injury in very pre-
term neonates: practical implications. Dev Med Child Neurol 53(Suppl 4):29–34
Woodward LJ (2006) Neonatal MRI to predict neurodevelopmental outcomes in preterm
infants. N Engl J Med 355:686–694
Woodward LJ (2006) Neonatal MRI to predict neurodevelopmental outcomes in preterm
infants. N Engl J Med 355:686–694
 8 Maturational Changes
of the Neonatal Brain

8.1 M
 aturational Processes

During the foetal and perinatal period, and early infancy impressive brain
growth and important maturational processes of the brain take place.
Because of this ongoing maturation, the neonatal and in particular the pre-
term brain is very vulnerable to abnormal development and injury. Patterns
of perinatal brain injury depend among others on the origin (i.e. traumatic,
hypoxic-ischaemic, inflammatory, haemorrhagic, toxic, metabolic) and
timing of the injury and on the developmental stage of the brain and thus
the postconceptional age of the foetus or newborn at the time of the event(s).
Certain CUS features are related to specific maturational phenomena,
and CUS images change with ongoing maturation (see also Part II). While
performing and assessing neonatal CUS examinations, one needs to be well
informed on normal brain maturation, maturational phenomena as
depicted by CUS and age-related patterns of perinatal brain injury.
Some of the normal maturational processes result in age-specific fea-
tures, many can be visualised with CUS and will be reviewed below.
Myelination, although one of the major maturational processes of the CNS
and depicted in detail by MRI, is not depicted by ultrasound and will not be
reviewed in this chapter.

8.2 G
 yration

Gyration starts in the second trimester of pregnancy. It progresses very rap-

idly in an ordered, predictable way. All primary sulci develop between 14
and 34 weeks gestation, and the process of gyration is completed around
© Springer Nature Switzerland AG 2019 195
G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
196 8 Maturational Changes of the Neonatal Brain

term. In extremely preterm infants (GA 24–26 weeks), the brain surface is
still very smooth and has an almost lissencephalic appearance (Fig. 8.1, see
also Fig. 4.1b and Part II), while around term age, the brain surface has an
almost mature appearance (Fig. 8.2; see also Fig. 4.1a).
Gyration and sulcation start around 14 weeks gestation with the forma-
tion of the lateral or Sylvian sulcus. In extremely preterm neonates (<24
weeks gestation), this is the only sulcus that can be recognised on ultra-
sound scans. The next sulci that can be distinguished are the calcarine,
parieto-occipital and cingulate sulci. The process of gyration can be fol-
lowed by ultrasonography, and the postmenstrual age of the infant can be
estimated from ultrasound images of the brain. CUS images obtained
around term age differ substantially from those obtained in very preterm
infants before TEA, mainly because of the progress in gyration (see Figs. 8.1
and 8.2 and Part II).
There are regional differences in gyral development: the posterior
regions of the brain develop much faster than the anterior regions. Thus, at
around 34 weeks of gestation, the frontal cortex is still smooth, while the
occipital cortex already shows obvious gyration.
In some infants born very prematurely, a reduced complexity in cortical
folding can be seen around TEA due to impaired brain growth (see Fig. 4.8).

8.3 G
 erminal Matrix

The germinal matrix is a transient structure from which the brain cells form
and mature. It is an abundant, highly cellular and vascular layer of subepen-
dymal tissue. During early gestation, it lines the entire wall of the lateral
ventricles and third ventricle. It produces neuroblasts and glioblasts and is
the origin of migrating neuronal (first trimester) and glial (second and third
trimesters) cells. Regression of the germinal matrix starts from 24 weeks
gestation onwards. After 33 weeks, residual germinal matrix cells remain in
the thalamo-caudate notch, the temporal horns and the lateral wall of the
occipital horns of the lateral ventricles. On MRI in foetuses and preterm
neonates, it is easily recognised as a prominent band of high signal on T1-
and low signal on T2-weighted images (Fig. 8.3). On CUS, the sites of the
8.3 Germinal Matrix 197

Fig. 8.1 CUS in two extremely preterm neonates (a and d GA 25+1 weeks, b and c GA
24+3 weeks) and a very preterm neonate (e GA 30 weeks), shortly after birth. (a, b) coro-
nal through, respectively, the body and trigone of the lateral ventricles, (c) and (e) mid-
sagittal and (d) parasagittal through the left insular area showing the very smooth
cortex and sparse gyration. In (a) and (d), the Sylvian fissure (arrow) is present. In (b),
the Sylvian fissure (arrow) and beginning formation of the calcarine fissure (green
arrow) can be recognised
198 8 Maturational Changes of the Neonatal Brain

Fig. 8.1 (continued) (c), the calcarine sulcus (green arrow) is seen. In (a), apart from
the Sylvian fissure, the hippocampal fissure is also depicted (asterisk). In (e), apart from
the now more mature calcarine sulcus, the cingulate sulcus (red arrow) is also seen.
Compare with Fig. 8.2. Note the wide subarachnoidal spaces, being a normal finding at
this age (green arrowheads in a and d).
8.3 Germinal Matrix 199

Fig. 8.1 (continued)

200 8 Maturational Changes of the Neonatal Brain

Fig. 8.2 (a, b) Coronal, (c) midsagittal and (d) parasagittal CUS scans in a full-term neo-
nate, showing advanced cortical folding. Compare with the same views in the preterm
neonates (see Fig. 8.1). The colours of the arrows and the asterisk indicating the sulci
correspond with the same structures as indicated in Fig. 8.1. White arrow indicates pre-
central sulcus, yellow arrow central sulcus
8.3 Germinal Matrix 201

Fig. 8.2 (continued)

202 8 Maturational Changes of the Neonatal Brain

Fig. 8.3 (a, c, e) Transverse T1-weighted MRI scans, (b, d, f) transverse T2-weighted MRI
scans. (a–d and g) high ventricular level, (e, f) basal ganglia level. (a, b) Extreme preterm
neonate, GA 25+6 weeks, scanned at PMA 28 weeks. The germinal matrix is clearly visible
as a band in the ventricular wall of high, respectively, low signal intensity on the T1- and
T2-weighted image (arrows). Note the motion artefact on the T2-weighted image. (c, d)
Very preterm neonate, GA 29 weeks, scanned at PMA 31+6 weeks. The germinal matrix
(arrows) is less extensive than in the younger infant. Also note the more advanced
cortical folding. (e–g) MRI at TEA in a preterm infant born at 33+6 weeks gestation. In (f),
some small remnants of the germinal matrix are visible in the temporal horns of the
lateral ventricles (arrow). Also note the advanced, almost mature cortical folding and
the high, respectively, low signal intensity in the PLIC (arrowheads in e and f), repre-
senting beginning myelination of the PLIC
8.3 Germinal Matrix 203

Fig. 8.3 (continued)

204 8 Maturational Changes of the Neonatal Brain

Fig. 8.3 (continued)

c

d
8.3 Germinal Matrix 205

Fig. 8.3 (continued)

e

f
206 8 Maturational Changes of the Neonatal Brain

Fig. 8.3 (continued)

g
8.3 Germinal Matrix 207

germinal matrix remnants can be distinguished as small areas of high

­echogenicity, mostly only visible around the thalamo-caudate notch on
parasagittal scans (Fig. 8.4). These small echogenic areas should be distin-
guished from GMH (Fig. 8.5; see also Fig. 6.1b).

Fig. 8.4 Parasagittal CUS scan through the left lateral ventricle in preterm infant, GA
32+2 weeks, postmenstrual age at scanning 34+6 weeks, showing a small area of
increased echogenicity around the thalamo-caudate notch (arrow), representing the
site of remnants of the germinal matrix (see also Fig. 8.5b). Note the prominent cingu-
late sulcus (red arrow). The calcarine sulcus (green arrow) is also shown
208 8 Maturational Changes of the Neonatal Brain

Fig. 8.5 CUS scans in extremely preterm neonate, GA 24+3 weeks performed on
­postnatal day 1 (a, b) and 2 (c, d). (a) and (c) coronal through the body of the lateral
ventricles, (b) and (d) parasagittal through left lateral ventricle. On postnatal day 1
(a, b), the thalamo-caudate notch (site of remnants of the germinal matrix) (blue arrow
in b) is clearly seen. Note the choroid plexus (green arrows). There is a small, vague
echogenicity in the left lateral ventricle (arrowheads), possibly presenting a beginning
GMH. On postnatal day 2 (c, d), there is now a small but obvious GMH (arrowheads).
The normal thalamo-caudate notch is no longer discernible
8.3 Germinal Matrix 209

Fig. 8.5 (continued)

210 8 Maturational Changes of the Neonatal Brain

8.4 C
 ell Migration

The first half of gestation is the period of neuronal cell proliferation and
migration. While neuronal cell migration is completed after 20 weeks gesta-
tion, glial cell migration continues until late gestation.
In the normal preterm neonate areas of subtle and symmetrical white
matter echogenicity can be recognised on CUS images, especially in the
frontal regions (Fig. 8.6). This physiological phenomenon represents glial
cell migration and should not be confused with non-physiological frontal
PVE (see also Fig. 5.6a–d).

Fig. 8.6 CUS on first postnatal day in extreme preterm neonate, GA 25+1 weeks. (a)
coronal scan through frontal lobes and (b) parasagittal scan through right insular area,
showing physiological areas of subtle and symmetrical echogenicity in the frontal
white matter (arrows)
8.5 Deep Grey Matter Changes 211

Fig. 8.6 (continued)

8.5 D
 eep Grey Matter Changes

During the preterm period, changes over time can be seen in the basal gan-
glia. In very preterm infants, these deep grey matter structures, especially
the putamen, often show diffuse, subtly increased echogenicity as compared
to the surrounding tissue (Fig. 8.7; see Fig. 4.5a, b). The echogenicity is seen
in about 90% of very preterm infants (GA < 32 weeks), fades with age and is
generally no longer seen after 1 month post-term.
This prematurity-related phenomenon should be distinguished from
pathological changes in the deep grey matter, typically occurring in
­(near)-term neonates after perinatal asphyxia. These changes may also be
subtle and diffuse but represent hypoxic-ischaemic injury and may be of
great clinical importance (see Fig. 4.5c, d). It should also be distinguished
from more localised or unilateral lesions in the thalami and/or basal gan-
glia, resulting from haemorrhage or infarction (see Fig. 4.5g, h).
212 8 Maturational Changes of the Neonatal Brain

Fig. 8.7 Extreme preterm neonate, GA 25+3 weeks, CUS on postnatal day 1. (a) coronal
scan through frontal lobes and (b) parasagittal scan through right lateral ventricle. The
basal ganglia are subtly and diffusely echogenic (arrows), a physiological phenome-
non at this age
8.6 Changes in Cerebrospinal Fluid Spaces 213

8.6 C
 hanges in Cerebrospinal Fluid Spaces

In the foetus and very preterm infant, the lateral ventricles may be wide and
asymmetrical (usually the left ventricle is wider than the right) with rela-
tively wide occipital horns (Fig. 8.8). Subarachnoidal spaces may also be
wide (see also Fig. 8.1a, b and d). Because of brain growth and fluid loss in
the first few days after birth, the cerebrospinal fluid spaces gradually
decrease (Fig. 8.9, compare with Fig. 8.1a, b and d).

Fig. 8.8 Same infant as in Fig. 8.5. (a) Coronal scan through the trigone of the lateral
ventricles and (b) and (c) parasagittal scans through, respectively, the right and left
lateral ventricle. The occipital horns are relatively wide (depicted in c), and the left ven-
tricle is wider than the right ventricle. Note the asymmetrical, bulky choroid plexus (red
arrows), a normal finding, especially in preterm neonates
214 8 Maturational Changes of the Neonatal Brain

Fig. 8.8 (continued)

8.6 Changes in Cerebrospinal Fluid Spaces 215

Fig. 8.9 Coronal CUS images in extreme preterm neonate, GA 25+3 weeks, postnatal
day 3. Due to fluid loss and brain growth, the subarachnoidal spaces become smaller
(compare with Fig. 8.1). Note again the bulky, echogenic choroid plexus in (b), being a
normal finding
216 8 Maturational Changes of the Neonatal Brain

After some conditions (such as extreme prematurity and hypoxic-­

ischaemic brain injury), the cerebrospinal fluid spaces remain or become
wide, even after term age (see Fig. 4.8), due to impaired brain growth.

Changes of brain maturation

• Increase in volume and weight
• Cortical folding
• Myelination (not depicted by CUS)
• Cell migration
• Germinal matrix involution
• Deep grey matter changes
• Decrease in cerebrospinal fluid spaces

Further Reading

Achiron R et al (2002) Cerebral lateral ventricular asymmetry: is this a normal ultrasono-

graphic finding in the fetal brain? Obstet Gynecol 89:233–237
Barkovich AJ, Mukherjee P (2012) Normal development of the neonatal and infant brain,
skull, and spine. In: Barkovich AJ, Raybaud C (eds) Pediatric neuroimaging. Lippincot
Williams & Wilkins, Wolters Kluwer, Philadelphia
Battin M, Rutherford M (2002) Magnetic resonance imaging of the brain in preterm
infants: 24 weeks’ gestation to term. In: Rutherford M (ed) MRI of the neonatal brain.
WB Saunders, London
Boardman JP et al (2007) Early growth in brain volume is preserved in the majority of
preterm infants. Ann Neurol 62:185–192
Boxma A et al (2005) Sonographic detection of the optic radiation. Acta Paediatr
94:1455–1461
Brouwer MJ et al (2010) Ultrasound measurements of the lateral ventricles in neonates:
why, how and when? A systematic review. Acta Paediatr 99:1298–1306
Brouwer MJ et al (2012) New reference values for the neonatal cerebral ventricles.
Radiology 262:224–233
Chi JG et al (1977) Gyral development of the human brain. Ann Neurol 1:86–93
Garel C et al (2001) Fetal cerebral cortex: normal gestational landmarks identified using
prenatal MR imaging. Am J Neuroradiol 22:184–189
de Goederen R et al (2017) Effect of preterm birth on echogenicity in basal ganglia.
Ultrasound Med Biol 43(10):2192–2199
Girard N et al (2007) MR imaging of brain maturation. J Neuroradiol 34:290–310
Further Reading 217

Griffiths PD et al (2010) Atlas of fetal and postnatal brain MRI. Saunders Elsevier,
Philadelphia
Horsch S et al (2005) Ultrasound diagnosis of brain atrophy is related to neurodevelop-
mental outcome in preterm infants. Acta Paediatr 94:1815–1821
Huang CC, Yeh TF (1991) Assessment of gestational age in newborns by neurosonogra-
phy. Early Hum Dev 25:209–220
Kinney, Volpe (2017a) Organizational events. In: Volpe’s neurology of the newborn, 6th
edn. Elsevier
Kinney, Volpe (2017b) Myelination events. In: Volpe’s neurology of the newborn, 6th edn.
Elsevier
van der Knaap MS et al (1996) Normal gyration and sulcation in preterm and term neo-
nates: appearance on MR images. Radiology 200:389–396
Leijser LM et al (2009) Frequently encountered cranial ultrasound features in the white
matter of preterm infants: correlation with MRI. Eur J Paediatr Neurol 13:317–326
Murphy NP et al (1989) Cranial ultrasound assessment of gestational age in low birth-
weight infants. Arch Dis Child 64:569–572
Naidich TP et al (1994) The developing cerebral surface. Preliminary report on the pat-
terns of sulcal and gyral maturation—anatomy, ultrasound, and magnetic resonance
imaging. Neuroimaging Clin N Am 4:201–240
Poduri, Volpe (2017c) Neuronal proliferation. In: Volpe’s neurology of the newborn, 6th
edn. Elsevier
Poduri, Volpe (2017d) Neuronal migration. In: Volpe’s neurology of the newborn, 6th
edn. Elsevier
Veyrac C et al (2006) Brain ultrasonography in the premature infant. Pediatr Radiol
36:626–635
van Wezel-Meijler G et al (1998) Magnetic resonance imaging of the brain in premature
infants during the neonatal period. Normal phenomena and reflection of mild ultra-
sound abnormalities. Neuropediatrics 29:89–96
van Wezel-Meijler G et al (2011) Diffuse hyperechogenicity of the basal ganglia and thal-
ami in preterm infants: a physiologic finding? Radiology 258:944–950
 9 Transcranial Doppler Sonography
in Neonates

One of the advantages of CUS is the possibility to study cerebral haemody-

namics. Transcranial Doppler sonography is an excellent modality for
assessment of the cerebral vasculature in the newborn infant and provides
useful information about cerebral vascular anatomy. Since it is non-invasive
and seen in real time, it is an ideal technique to study blood flow patterns
over time and in various clinical situations. The assessment of cerebral
blood flow velocities enables the detection of abnormal flow patterns, may
provide information regarding the risk of brain injury (for example IVH)
and can play a role in determining the severity of brain damage (e.g. in cases
with hypoxic-ischaemic encephalopathy).

9.1 M
 achine Settings

Modern ultrasound systems have settings for colour Doppler sonography.

The layout between machines may vary, and it is important to know which
knobs are used to obtain the colour Doppler image box (CDI) on the screen,
how to move the box, obtain the pulsed wave Doppler signal (PW) and
place the flow sample volume on the artery under investigation (Fig. 9.1a–e).
Most machines have settings to trace the signal and place the cursors for
automatic measurement (Fig. 9.1f).

© Springer Nature Switzerland AG 2019 219

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
220 9 Transcranial Doppler Sonography in Neonates

Fig. 9.1 (a) Example of ultrasound machine control panel with knobs to obtain the CDI
and PW Doppler signal on the screen. Ultrasound images with (b) colour Doppler box
(green box) and (c) the sample volume (blue arrow) placed within the anterior cerebral
artery. Note the standard angle of insonation (white arrow). (d) The angle of insonation
is slightly changed (white arrow), the standard size of the sample volume in this setting
is still 2 mm (blue arrow); both also indicated within blue circle in c and d. (e) Sample
volume size now changed to 5 mm (blue arrow, blue circle in e). (f) Automatic measure-
ment of flow velocities and indices
9.1 Machine Settings 221

Fig. 9.1 (continued)

222 9 Transcranial Doppler Sonography in Neonates

Fig. 9.1 (continued)

9.2 Performing Doppler Examination 223

9.2 P
 erforming Doppler Examination

9.2.1 I maging Cerebrovascular Anatomy

Transcranial Doppler sonography can be performed using the anterior fon-

tanelle as well as additional acoustic windows, depending on the location of
the vessels of interest. Good-quality images of vessels can be obtained with
the micro CV probe. The high-frequency LA transducer is very useful to
visualise superficial vessels at or near the brain’s convexity (e.g. the superior
sagittal and transverse sinuses).
The larger arteries and their smaller branches as can be visualised by
Doppler sonography are listed in Box 9.1 (Figs. 9.2, 9.3, and 9.4), including the
acoustic window(s) most suitable for visualisation of these vessels. Likewise,
cerebral veins and sinuses are listed in Box 9.2 (Figs. 9.5, 9.6, and 9.7).

Box 9.1 Cerebral arteries

Large arteries and branches visualised during Acoustic
CUS examination window
• Internal carotid artery • AF, TW
    – Anterior choroidal artery
    – Posterior communicating artery
• Basilar artery • AF, TW, MF
• Anterior cerebral artery • AF, TW
   – Pericallosal artery
   – Callosal marginal artery
    – Frontal artery branches
    – Heubner’s artery
• Middle cerebral artery • AF, TW
    – Lenticulostriate arteries
    – Insular arteries
    – Cortical arteries
• Posterior cerebral artery • AF, TW, MF
   – Thalamic arteries
    – Choroidal artery
   – Supracerebellar artery
AF anterior fontanelle, PF posterior fontanelle, TW temporal window, MF mastoid ­fontanelle
224 9 Transcranial Doppler Sonography in Neonates

Fig. 9.2 Examples of coronal colour Doppler images demonstrating (a) the circle of
Willis, with the internal carotid artery (ICA), main branch of the middle cerebral artery
(MCA) and the anterior cerebral artery (ACA), (b) the MCA with its striate branches and
insular segment, (c) the basilar artery, (d) the posterior cerebral artery (PCA) coming
from the basilar artery, (e) MCA with its striate branches and insular segment as visual-
ised by (non-directional) microvascular imaging
9.2 Performing Doppler Examination 225

Fig. 9.2 (continued)

226 9 Transcranial Doppler Sonography in Neonates

Fig. 9.2 (continued)

Fig. 9.3 Examples of sagittal colour Doppler images demonstrating (a, b) on (almost)
midsagittal views the ICA, basilar artery, ACA and its branches, the pericallosal artery
(aPC), the callosal marginal artery (aCM) and frontal internal arteries (aFI); and on para-
sagittal views (c) striate branches of MCA and (d) insular segment of MCA
9.2 Performing Doppler Examination 227

Fig. 9.3 (continued)

228 9 Transcranial Doppler Sonography in Neonates

Fig. 9.3 (continued)

Fig. 9.4 Examples of colour Doppler images obtained though the temporal window
(a) and mastoid fontanelle (b–d) demonstrating (a) circle of Willis with ACA, MCA and
PCA; (b, c) also showing superior cerebellar artery (SCA) and (d) branches of SCA
within cerebellum
9.2 Performing Doppler Examination 229

Fig. 9.4 (continued)

230 9 Transcranial Doppler Sonography in Neonates

Fig. 9.4 (continued)

Box 9.2 Cerebral veins and sinuses

Large veins and sinuses visualised during CUS Acoustic
examination window
• Superior sagittal sinus • AF, PF
• Inferior sagittal sinus • AF
• Internal cerebral vein • AF
– Terminal veins
– Septal veins
– Choroidal veins
  – Thalamic veins
• Vein of Galen • AF, PF
• Straight sinus • AF, MF
• Torcular Herophili • AF, PF, MF
• Sigmoid sinuses • MF
• Transverse sinuses • MF, AF
AF anterior fontanelle, PF posterior fontanelle, TW temporal window, MF mastoid fontanelle
9.2 Performing Doppler Examination 231

Fig. 9.5 Examples of midsagittal colour Doppler images demonstrating venous flow in
(a) the superior sagittal sinus (SSS), straight sinus (ST), (b) inferior sagittal sinus (ISS),
internal cerebral vein (ICV) and vein of Galen (VOG), (c) Image obtained with LA trans-
ducer showing Power Doppler with (directional) flow signal in the SSS and small superfi-
cial cortical veins. To enhance signal quality, the probe is angled slightly backwards, and
the depth of the image is reduced, (d) Flow signal in the posterior part of the SSS, of note
the focus point is aimed at the posterior region (blue circle) to enhance signal quality
232 9 Transcranial Doppler Sonography in Neonates

Fig. 9.5 (continued)

9.2 Performing Doppler Examination 233

Fig. 9.6 Examples of coronal colour Doppler images demonstrating venous flow in (a)
the ICV, (b) terminal veins (TV) and (c) transverse sinuses (TRV)
234 9 Transcranial Doppler Sonography in Neonates

Fig. 9.6 (continued)

Fig. 9.7 Examples of coronal (a–c) and transverse (d) images obtained from the mas-
toid fontanelle demonstrating (a) the echolucent triangle (b) colour Doppler image
and (c) venous flow pattern of the ipsilateral TRV and (d) colour Doppler image of the
­contralateral TRV
9.2 Performing Doppler Examination 235

Fig. 9.7 (continued)

236 9 Transcranial Doppler Sonography in Neonates

Fig. 9.7 (continued)

For details on the anatomy of the cerebral arterial and venous system, see
Govaert [1], Miller [2] and Raets [3].

9.2.2 Assessing Cerebral Blood Flow Patterns and Velocities

When performing Doppler measurements, it is important that the baby is

comfortable, not crying or making manoeuvres that might alter flow, espe-
cially while venous patterns are assessed, since these may be affected by
movements. It is also important to be aware of clinical conditions that may
alter cerebral blood flow velocity (see Sect. 9.3.1).
Doppler measures velocity and not flow. The diameter of the vessels is
generally too small to calculate flow.
In cerebral arteries, blood flow should always be forward; backflow is
abnormal and seen in various clinical conditions.
While performing colour Doppler imaging, a colour map depicting
movement is superimposed on the grey-scale ultrasound image (Figs. 9.7,
9.8, and 9.9). This colour map shows blood flow with directional informa-
tion. Blood flowing towards the probe is represented by a red signal, while
9.2 Performing Doppler Examination 237

blood flowing away from the probe is represented by a blue signal. Many
modern machines also have power Doppler and microvascular imaging
techniques. These techniques are more sensitive and will detect smaller ves-
sels but sometimes lack directional information (Fig. 9.2e).

To perform an arterial velocity recording (Figs. 9.8 and 9.9):

1. Firstly, a large artery should be selected.
2. Subsequently, the colour map is placed over the area of interest (Fig. 9.8a).
It is important to perform measurements on a vessel running parallel to
the line of insonation (Fig. 9.8b). This is because the angle between the
Doppler ultrasound beam (as indicated by the cursor line) and the axis
of the blood vessel will affect the Doppler frequency shift and therefore
the size of the waveform. The higher the angle, the smaller the waveform
and the poorer the quality of the spectra. Although the Doppler indices
are almost angle independent, the angle of insonation should therefore
preferably be kept as close to zero as possible (Fig. 9.8b). This can be
achieved by choosing the most appropriate acoustic window (see Box
9.1) and by angling the probe so the line of insonation is (almost) parallel
with the line of the vessel. If necessary, the angle of insonation can be
further adapted by a slight rotation of the cursor (Fig. 9.1c, d). From the
anterior fontanelle, the flow velocities in the anterior cerebral, perical-
losal, internal carotid and basilar arteries and also the superior and
straight sinuses can be assessed (Fig. 9.8). The middle cerebral artery is
best assessed from the temporal window (Fig. 9.9).
3. The Doppler sample volume is then placed over the vascular lumen
(Fig. 9.8b, c), and the waveforms are recorded. The size of the sample vol-
ume can be altered to fit the size of the vessel (Fig. 9.1d, e). The flow veloc-
ity scale can be altered, so the spectra fill around half the screen (Fig. 9.9b,
c). Some machines optimise this automatically. For proper measurements,
it is important to have good-quality spectra with fairly uniform signals.
4. The peak systolic- and end-diastolic velocities are then identified with
cursors, and the Doppler indices are generated. A mean of three to five
cardiac cycles is usually taken for the measurement (Fig. 9.8c). Most
ultrasound systems will semi-automatically generate these indices.
238 9 Transcranial Doppler Sonography in Neonates

Fig. 9.8 Doppler flow measurements on anterior fontanelle midsagittal (a–c) and
coronal (d) views. (a) The colour box (green box) is placed on the image, and the ACA
and aPC can be identified. (b) The flow sample is placed over the ACA. Note that the
angle of insonation is in line with the axis of the vessel (arrow). (c) The flow sample is
placed over the aPC, Doppler waves are seen below, and flow velocities and indices are
calculated over four cardiac cycles. The RI is 0.72 (blue circle). (d) Same infant, Doppler
measurement in the ICA on a coronal ultrasound image. The RI is 0.73
9.2 Performing Doppler Examination 239

Fig. 9.8 (continued)

240 9 Transcranial Doppler Sonography in Neonates

Fig. 9.9 Doppler flow measurements of the MCA through the temporal window. (a)
The colour box is placed on the image, and both MCA can be identified. (b) The flow
sample (arrow) is placed over the MCA. Note the angle of insonation is in line with the
axis of the vessel. The flow waves are visible below; however, the flow velocity scale
should be adapted. (c) After adaptation of the scale (blue circle), the flow waves are
nicely and completely shown, and measurements can be performed
9.2 Performing Doppler Examination 241

Fig. 9.9 (continued)

The most common Doppler index used is the resistance index (RI),
defined as:

peak systolic velocity - end diastolic velocity

peak systolic velocity

It is important to realise that the RI differs to some degree in arteries of

different calibres. Serial measurements are therefore only useful if per-
formed in the same vessel at the same location. For a general measurement,
the anterior cerebral artery is preferred as it is easily accessible from the
anterior fontanelle with a low angle of insonation and therefore with good
reproducibility. Normal RI values range between 0.65 and 0.85. Reference
values of indices in different vessels are available for preterm and full-term
infants.
242 9 Transcranial Doppler Sonography in Neonates

9.3 C
 linical Application of Doppler Assessment

9.3.1 C
 linical Importance of Assessing Cerebral Blood
Flow Velocity

Several conditions may affect the flow velocity patterns and RI:

• Systemic blood pressure changes and hypovolaemia in the context of

impaired cerebrovascular autoregulation. Especially marked beat-to-
beat fluctuations and backward arterial flow are worrisome findings and
may precede IVH (Fig. 9.10).
• A haemodynamically important patent ductus arteriosus may cause
waveforms with high peak systolic velocity and absent or negative end-­
diastolic velocity, due to a significant left-to-right shunt with retrograde
diastolic flow. The same pattern can be seen in ductal-dependent con-
genital heart defects (Fig. 9.11).

Fig. 9.10 CUS on first postnatal day in a preterm infant with severe respiratory distress,
hypovolemia and refractory hypotension, showing an abnormal irregular shape of the
arterial flow pattern in the ACA with beat-to-beat variation and diastolic backflow
9.3 Clinical Application of Doppler Assessment 243

Fig. 9.11 (a, b) CUS on day 2 in preterm infant born at 29 weeks gestation. Doppler
flow measurement in the ACA from the anterior fontanelle (a) and MCA from the tem-
poral window (b) demonstrate high peak flow velocity in combination with almost
absent diastolic flow in each cardiac cycle possibly due to a patent ductus arteriosus.
The RI is therefore almost 1. (c) CUS in an infant with pulmonary atresia. Doppler flow
measurement in the ACA shows diastolic backflow due to the patent ductus arteriosus
which is required for the pulmonary circulation
244 9 Transcranial Doppler Sonography in Neonates

Fig. 9.11 (continued)

9.3 Clinical Application of Doppler Assessment 245

• Changes in carbon dioxide levels may affect cerebral blood flow.

High pCO2 levels can cause vasodilatation and higher blood flow veloci-
ties, while low pCO2 levels may cause vasoconstriction and low blood
flow velocities.
• Increased intracranial pressure, for example in PHVD can cause hae-
modynamic alterations with an increase in RI reflecting high peak sys-
tolic and low end-diastolic velocities. This may improve after lumbar
or ventricular taps or permanent shunting (Fig. 9.12; see also Chap. 4
and Fig. 5.1).
• Respiratory distress and insufficiently synchronised artificial ventilation
can cause haemodynamic alterations, resulting in irregular waveforms.
Venous patterns are often somewhat affected by normal breathing, but
marked or extreme fluctuations in venous flow patterns are abnormal
and are associated with an increased risk of IVH (Fig. 9.13).

Fig. 9.12 CUS in preterm infant with bilateral grade III IVH and PHVD. Doppler flow mea-
surement on day 14 demonstrating high peak flow velocity in combination with low end-
diastolic velocity and high RI values, likely due to increased intracranial pressure. The infant
was treated with spinal taps and a ventriculoperitoneal shunt (see also Chap. 5, Fig. 5.1)
246 9 Transcranial Doppler Sonography in Neonates

Fig. 9.13 Fluctuating venous flow patterns. (a, b) Preterm infant with normal fluctua-
tion of venous flow in the transverse sinus due to breathing and hiccups, as seen from
the anterior (a) and mastoid (b) fontanelle. (c) Abnormal fluctuations in venous flow
due to severe respiratory insufficiency in combination with cardiac failure in a full-term
neonate with hydrops and perinatal asphyxia
9.3 Clinical Application of Doppler Assessment 247

Fig. 9.13 (continued)

• Hypoxic-ischaemic encephalopathy
Moderate to severe perinatal asphyxia may affect the reactivity of the
cerebral vascular bed. After initial hypoperfusion during the hypoxic
event, there is a phase of compensatory vascular dilatation and a decrease
in vascular resistance, characterised by hyperperfusion. This so-called
luxury perfusion can be recognised on CUS starting from 6 to 24 h after
the event. Initially, the reduction in cerebrovascular resistance helps to
maintain or restore oxygen delivery to the brain, but in severe cases with
impaired autoregulation and vasoparalysis, the hyperperfusion contin-
ues and is unresponsive to changes in blood pressure and pCO2.
Measurement of the cerebral blood flow velocity shows a drop in RI,
mainly caused by a rise in diastolic flow velocity (Fig. 9.14). The RI value
correlates with the severity of brain injury, with values <0.55 being
abnormal and predictive of cerebral injury and abnormal outcome. In
the context of hypothermia treatment, a low RI is less predictive of poor
outcome, probably because hypothermia affects cerebral circulation
and/or protects the brain. However, a persisting low RI after rewarming
remains an indicator of poor outcome.
248 9 Transcranial Doppler Sonography in Neonates

Fig. 9.14 Coronal (a) and sagittal (b, c) ultrasound images on fourth postnatal day in
full-term infant with severe perinatal asphyxia demonstrating (a, b) increased echo-
genicity in basal ganglia and thalami (arrows) with hypo-echogenic PLIC (green arrows)
and (c) luxury perfusion pattern (RI 0.55) in the aPC
9.3 Clinical Application of Doppler Assessment 249

Fig. 9.14 (continued)

250 9 Transcranial Doppler Sonography in Neonates

9.3.2 C
 linical Importance of Assessing Cerebrovascular
Anatomy

Knowledge on the normal cerebrovascular anatomy enables recognition of

abnormalities. These abnormalities include:

• Occlusion or reduced flow signal in one of the main arteries or its branches
may be seen in early stages of arterial stroke, while luxury (or hyper-)
perfusion is sometimes seen in later stages (Fig. 9.15).
• Occlusion or reduced flow in one of the sinuses reflecting cerebral sinove-
nous thrombosis. This condition is often clinically silent, but not uncom-
mon in the sick and/or preterm infant. Doppler sonography is highly
specific to rule out cerebral sinovenous thrombosis (Figs. 9.5 and 9.7).
• Vascular anomalies such as the vein of Galen malformation and other
arteriovenous malformations can be detected by Doppler sonography
(Figs. 9.16 and 9.17). In some infants, an asymptomatic developmental
venous anomaly may be detected as incidental finding.
• Some rare brain tumours, such as plexus papilloma, may show intensive
blood supply.
9.3 Clinical Application of Doppler Assessment 251

Fig. 9.15 CUS on fourth postnatal day in a full-term infant with left MCA infarction. (a)
Coronal ultrasound image demonstrating increased echogenicity in the left MCA terri-
tory. (b, c) Images through the right temporal window with flow pattern in the right (b)
and left (c) MCA demonstrating luxury perfusion pattern in the left MCA
252 9 Transcranial Doppler Sonography in Neonates

Fig. 9.15 (continued)

Fig. 9.16 Coronal (a, c) and midsagittal (b, d) ultrasound images on fifth postnatal day in
a full-term infant with vein of Galen malformation. (a, b) Demonstrating a large echolu-
cent midline structure. (c, d) Colour Doppler images demonstrate highly turbulent flow
within the structure. This is typical for a vein of Galen malformation and differentiates this
condition from, i.e. an arachnoid or velum interpositum midline cyst (see also Fig. 9.17)
9.3 Clinical Application of Doppler Assessment 253

Fig. 9.16 (continued)

254 9 Transcranial Doppler Sonography in Neonates

Fig. 9.16 (continued)

Fig. 9.17 Full-term infant with cavum velum interpositum cyst, shown on coronal (a)
and midsagittal (b) images as a large echolucent midline structure. Colour Doppler
image (c) shows the ICV anterior and inferior to the cyst. There is no flow demonstrable
within the cystic structure (compare with Fig. 9.16)
9.3 Clinical Application of Doppler Assessment 255

Fig. 9.17 (continued)

256 9 Transcranial Doppler Sonography in Neonates

Box 9.3 Highlights of Doppler sonography

Features of Doppler sonography Clinical context
Real time
Enables:
Evaluation of cerebral blood flow • Low blood pressure
patterns over time and in various • Hypovolemia
clinical conditions • Patent ductus arteriosus
• Hyper-, hypocarbia
• Severe respiratory disease
• Suboptimal artificial ventilation
• Increased intracranial pressure
• Hypoxic ischaemic encephalopathy
Assessment of cerebral vasculature • Arterial stroke
• Cerebral sinovenous thrombosis
• Vascular anomalies
May provide information regarding • Development of IVH
risk of brain injury
May contribute to prognosis Hypoxic ischaemic encephalopathya
a
In hypothermia after rewarming

References

1. Govaert P (2009) Sonographic stroke templates. Semin Fetal Neonatal Med 14:284–298
2. Miller E et al (2014) Color Doppler US of normal cerebral venous sinuses in neonates:
a comparison with MR venography. Pediatr Radiol 42:1070–1079
3. Raets M et al (2015) Brain vein disorders in newborn infants. Dev Med Child Neurol
57:229–240

Further Reading

Couture A et al (2001) Advanced cranial ultrasound: transfontanellar Doppler imaging in

neonates. Eur Radiol 2001(11):2399–2410
Dean LM et al (1995) The intracranial venous system in infants: normal and abnormal
findings on duplex and color Doppler sonography. AJR Am J Roentgenol 164:151–156
Further Reading 257

Ecury-Goossen GM et al (2015) State of the art cranial ultrasound imaging in neonates.

J Vis Exp 96
Elstad M et al (2011) Cerebral Resistance Index is less predictive in Hypothermic enceph-
alopathic newborns. Acta Paediatr 100(10):1344–1349
Forster DE et al (2018) Cerebral blood flow velocities and cerebrovascular resistance in
normal-term neonates in the first 72 hours. J Paediatr Child Health 2018(54):61–68
Gerner GJ et al (2016) Transfontanellar duplex brain ultrasonography resistive indices as
a prognostic tool in neonatal hypoxic-ischemic encephalopathy before and after treat-
ment with therapeutic hypothermia. J Perinatol 36(3):202–206
Grant EG et al (1987) Cranial duplex sonography of the infant. Radiology 163:177–185
Horsch S et al (2014) Developmental venous anomaly in the newborn brain.
Neuroradiology 56:579–588
Ikeda T et al (2015) Changes in the perfusion waveform of the internal cerebral vein and
intraventricular haemorrhage in the acute management of extremely low-birth-weight
infants. Eur J Pediatr 174:331–338
Perlman JM et al (1983) Fluctuating cerebral blood flow velocity in respiratory distress
syndrome. N Engl J Med 309:204–209
Raets MM et al (2013) Serial cranial US for detection of cerebral sinovenous thrombosis
in preterm infants. Radiology 269:879–886
Romagnoli C et al (2006) Neonatal color Doppler US study: normal values of cerebral
blood flow velocities in preterm infants in the first months of life. Ultrasound Med
Biol 32(3):321–331
Skranes JH et al (2014) Hypothermia makes cerebral resistance index a poor prognostic
tool in encephalopathic newborns. Neonatology 106:17–23
PART II ULTRASOUND ANATOMY
OF THE NEONATAL BRAIN
260 PART II Ultrasound Anatomy of the Neonatal Brain

In part II, the ultrasound anatomy of the neonatal brain is demonstrated.

All the ultrasound images presented in this part are normal, unless
stated otherwise. For most presented planes at least two ultrasound images
are shown: one or two examples of very preterm neonates and one of a full-
term neonate, thus showing maturational changes. Exceptions are Figs. 12
and 13, where only examples of very preterm neonates are shown.
The illustrations represent the outlines of the matching ultrasound
images, the numbers corresponding to the numbers listed in Table 1.

Table 1 List of anatomical structures

Structure Shown in figures
1 Interhemispheric fissure Figs. 10.4, 10.5, 10.6, 10.7, 10.8, 10.9
2 Frontal lobe Figs. 10.4, 10.5, 10.6, 11.5, 11.6, 13.3c
3 Skull Figs. 10.4, 10.5, 10.6, 10.7, 10.8, 10.9, 11.4,
11.5, 11.6, 11.7, 14.3d, 14.6b
4 Orbit Fig. 10.4
5 Frontal horn of lateral Figs. 10.5, 10.6, 11.5
ventricle
6 Caudate nucleus Figs. 10.5, 10.6, 10.7, 11.5
7 Basal ganglia Figs. 10.5, 10.6, 10.7, 11.5
8 Temporal lobe Figs. 10.5, 10.6, 10.7, 11.5, 11.6, 12.4b,
12.8b, 13.3, 14.3b, d, 14.6b–e
9 Sylvian fissure Figs. 10.5, 10.6, 10.7, 10.8, 11.6, 11.7
10 Corpus callosum Figs. 10.5, 10.6, 10.7, 10.8b, 11.4, 12.7b
11 Cavum septum Figs. 10.5, 10.6, 10.7b, 11.4
pellucidum
12 Third ventricle Figs. 10.6, 10.7c, 11.4, 12.7b, 13.3b
* Choroid plexus in third Fig. 10.6b
ventricle
13 Cingulate sulcus Figs. 10.6, 10.8c, 10.9c, 11.4c, 11.5d
14 Body of lateral ventricle Figs. 10.7, 10.8, 11.5, 12.4b, 12.8b, 14.3d
15 Choroid plexus Figs. 10.7, 10.8, 11.5, 12.4b, 12.8b, 14.3d
16 Thalamus Figs. 10.7, 11.5, 12.8b
17 Parahippocampal gyrus Figs. 10.7, 11.5c, d, 13.3b, c
18 Mesencephalon Figs. 10.7, 11.4, 12.4b, 12.7b, 13.3, 14.3b,
c, 14.6b, c
PART II Ultrasound Anatomy of the Neonatal Brain 261

Table 10.1 (continued)

Structure Shown in figures
19 Cerebellum Figs. 10.7, 13.3c, d, 14.6b, c
19a Cerebellar hemisphere Figs. 10.7, 11.5, 12.4c, d, 14.3, 14.6d–g
19b Cerebellar vermis Figs. 10.7, 11.4, 12.4c, d, 12.7b, 13.3b,
14.3, 14.6d–g
20 Temporal horn of lateral Figs. 10.7, 11.5, 12.8b, 13.3, 14.3b, 14.6d
ventricle
21 Tentorial area Figs. 10.7, 12.4c, d, 14.3b, d, e
22 Parietal lobe Figs. 10.7, 10.8, 10.9, 11.5, 11.6, 12.4b,
12.8b, 14.3d
23 Occipital lobe Figs. 10.8, 10.9, 11.5, 11.6, 12.4, 12.8b
24 Cavum vergae Figs. 10.8b, 11.4b
25 Calcarine fissure Figs. 10.8, 10.9, 11.4, 12.4c, d, 12.7b, 12.8b
26 Parieto-occipital fissure Figs. 10.9c, 11.4, 11.5c, 12.7b
27 Pons Figs. 11.4, 12.7b, 14.6d–f
28 Tectal (quadrigeminal) Figs. 11.4, 12.7b
plate
29 Medulla oblongata Figs. 11.4, 12.7b, 14.6g
30 Fourth ventricle Figs. 11.4, 12.7b, 14.3b, c, 14.6d, e
31 Cisterna magna Figs. 11.4, 12.7b, 14.3, 14.6d–g
32 Interpeduncular cistern Figs. 11.4, 12.4b, 13.3b, c, 14.6b
33 Fornix Figs. 11.4
34 Mesencephalic aqueduct Figs. 11.4, 12.4b, 12.7b, 13.3b, c
35 Occipital horn of lateral Figs. 12.4c, 12.8b, 14.3b
ventricle
36 Insular area Figs. 11.6, 11.7
37 Insular sulci Fig. 11.6c
38 Central sulcus Figs. 11.6c, 11.7c
39 Postcentral sulcus Figs. 11.6c, 11.7c
40 Precentral sulcus Figs. 11.6c, 11.7c
41 Cerebral peduncle Figs. 13.3, 14.6b
42 Circle of Willis Fig. 13.3d
42a Anterior cerebral artery Fig. 13.3d
(ACA)
(continued)
262 PART II Ultrasound Anatomy of the Neonatal Brain

Table 10.1 (continued)

Structure Shown in figures
42b Middle cerebral artery Fig. 13.3d
(MCA)
42c Posterior cerebral artery Fig. 13.3d
(PCA)
43 Foramen of Magendie Figs. 14.3c, 14.6f
44 Cerebellar folia Figs. 14.3c, e, 14.6c, e, g
 10 Coronal Planes Anterior Fontanelle

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264 10 Coronal Planes Anterior Fontanelle

Fig. 10.1 Probe positioning for coronal planes

10 Coronal Planes Anterior Fontanelle 265

Fig. 10.2 Drawing of probe positioning to obtain the standard coronal planes
266 10 Coronal Planes Anterior Fontanelle

1
5

2 4
3

Fig. 10.3 The six standard coronal planes

10 Coronal Planes Anterior Fontanelle 267

Fig. 10.4 (a) First coronal plane at the level of the frontal lobes. (b and c) Ultrasound
scans of the first coronal plane at the level of the frontal lobes. (b) Preterm neonate, GA
25+3 weeks, first postnatal day. Image shows subtle symmetrical, physiological echo-
genicity of the frontal white matter (see also Part I Chaps. 5 and 8). (c) Full-term
neonate.
268 10 Coronal Planes Anterior Fontanelle

Fig. 10.4 (continued)

10 Coronal Planes Anterior Fontanelle 269

Fig. 10.4 (continued) 1: interhemispheric fissure; 2: frontal lobe; 3: skull; 4: orbit

270 10 Coronal Planes Anterior Fontanelle

Fig. 10.5 (a) Second coronal plane at the level of the frontal horns of the lateral ven-
tricles. (b and c) Ultrasound scans of the second coronal plane at the level of the frontal
horns of the lateral ventricles.
10 Coronal Planes Anterior Fontanelle 271

2
1
5
10
6
11
9
7

8
3

Fig. 10.5 (continued) (b) Preterm neonate, GA 25+1 weeks, first postnatal day. Image
shows small, symmetrical echogenic areas in the frontal white matter and subtle,
symmetrical echogenicity of the caudate nuclei: physiological findings in preterm
neonates before TEA (see also Part I Chap. 8). (c) Full-term neonate. Image shows
narrow lateral ventricles. This is a normal finding if the brain parenchyma looks normal,
especially during the first postnatal days.
272 10 Coronal Planes Anterior Fontanelle

1
2

5
10
6
11

7 9

8 3

Fig. 10.5 (continued) 1: interhemispheric fissure; 2: frontal lobe; 5: frontal horn of

lateral ventricle; 6: caudate nucleus; 7: basal ganglia; 8: temporal lobe; 9: sylvian fissure;
10: corpus callosum; 11: cavum septum pellucidum
10 Coronal Planes Anterior Fontanelle 273

Fig. 10.6 (a) Third coronal plane at the level of foramen of Monro and the 3rd ventricle.
(b and c) Ultrasound scans of the third coronal plane at the level of the frontal horns of
the lateral ventricles. (b) Preterm neonate, GA 25+1 weeks, first postnatal day.
(c) Full-­term neonate.
274 10 Coronal Planes Anterior Fontanelle

2 1
13
10

5
6
11
7
*
12 9

3
8

Fig. 10.6 (continued)

10 Coronal Planes Anterior Fontanelle 275

2
13
10 5

11 6
12
7 9

Fig. 10.6 (continued) 1: interhemispheric fissure; 2: frontal lobe; 3: skull; 5: frontal

horn of lateral ventricle; 6: caudate nucleus; 7: basal ganglia; 8: temporal lobe; 9: sylvian
fissure; 10: corpus callosum; 11: cavum septum pellucidum; 12: third ventricle;
*: choroid plexus in third ventricle; 13: cingulate sulcus
276 10 Coronal Planes Anterior Fontanelle

Fig. 10.7 (a) Fourth coronal plane at the level of the body of the lateral ventricles.
(b and c) Ultrasound scans of the fourth coronal plane at the level of the body of the
lateral ventricles. (b) Preterm neonate, GA 24+3 weeks, first postnatal day. (c) Full-term
neonate.
10 Coronal Planes Anterior Fontanelle 277

22 14

10
6
9
15

7 11

20 16

18
17
21
8
19b
19a
3

Fig. 10.7 (continued)

278 10 Coronal Planes Anterior Fontanelle

1
10

22 14

6 15

7 9

16 12

20

17 18

21
8

19a 19b

Fig. 10.7 (continued) 1: interhemispheric fissure; 3: skull; 6: caudate nucleus; 7: basal

ganglia; 8: temporal lobe; 9: sylvian fissure; 10: corpus callosum; 11: cavum septum
pellucidum; 12: third ventricle; 14: body of lateral ventricle; 15: choroid plexus;
16: thalamus; 17: parahippocampal gyrus; 18: mesencephalon; 19: cerebellum;
19a: cerebellar hemisphere; 19b: cerebellar vermis; 20: temporal horn of lateral
ventricle; 21: tentorial area; 22: parietal lobe
10 Coronal Planes Anterior Fontanelle 279

Fig. 10.8 (a) Fifth coronal plane at the level of the trigone of the lateral ventricles.
(b and c) Ultrasound scans of the fifth coronal plane at the level of the trigone of the
lateral ventricles. (b) Preterm neonate, GA 24+3 weeks, first postnatal day. (c) Full-term
neonate. Note the subtle, linear echogenicity, running parallel to the lateral ventricles:
a normal finding in preterm and full-term neonates.
280 10 Coronal Planes Anterior Fontanelle

14

24 9

10 22

15 25

23

Fig. 10.8 (continued)

10 Coronal Planes Anterior Fontanelle 281

22

14

10 9

15
25

23
3

Fig. 10.8 (continued) 1: interhemispheric fissure; 3: skull; 9: sylvian fissure; 10: corpus
callosum; 14: body of lateral ventricle; 15: choroid plexus; 22: parietal lobe; 23: occipital
lobe; 24: cavum vergae; 25: calcarine fissure
282 10 Coronal Planes Anterior Fontanelle

Fig. 10.9 (a) Sixth coronal plane through the parieto-occipital lobes. (b and c)
Ultrasound scans of the sixth coronal plane at the level of the parieto-occipital lobes.
(b) Preterm neonate, GA 26 weeks, postnatal day 8. (c) Full-term neonate, GA 40 weeks,
postnatal day 8.
10 Coronal Planes Anterior Fontanelle 283

22

23 25

Fig. 10.9 (continued)

284 10 Coronal Planes Anterior Fontanelle

13 22

26

23
25

Fig. 10.9 (continued) 1: interhemispheric fissure; 3: skull; 13: cingulate sulcus; 22: pari-
etal lobe; 23: occipital lobe; 25: calcarine fissure; 26: parieto-occipital fissure
 11 Sagittal Planes Anterior Fontanelle

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available to authorized users.

© Springer Nature Switzerland AG 2019 285

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286 11 Sagittal Planes Anterior Fontanelle

Fig. 11.1 Probe positioning for sagittal planes

11 Sagittal Planes Anterior Fontanelle 287

Fig. 11.2 Drawing of probe positioning to obtain the standard sagittal planes
288 11 Sagittal Planes Anterior Fontanelle

5a 5 4 3 2 1 1a

Fig. 11.3 The five standard sagittal planes. Lines 1a and 5b represent extreme para-
sagittal planes
11 Sagittal Planes Anterior Fontanelle 289

Fig. 11.4 (a) Midsagittal plane through third and fourth ventricle, corpus callosum
and cerebellar vermis. (b and c) Ultrasound scans of midsagittal plane. (b) Preterm
neonate, GA 24+3 weeks, first postnatal day. (c) Full-term neonate, GA 40 weeks, post-
natal day 8.
290 11 Sagittal Planes Anterior Fontanelle

10 33

11 24
28

12 26

18 25
32 34
27 30
29 19b
31
3

Fig. 11.4 (continued)

11 Sagittal Planes Anterior Fontanelle 291

13
33
10
11 26

12 25
32 28
18 34
27
30

29 19b
31
3

Fig. 11.4 (continued) 3: skull; 10: corpus callosum; 11: cavum septum pellucidum;
12: third ventricle; 13: cingulate sulcus; 18: mesencephalon; 19b: cerebellar vermis;
24: cavum vergae; 25: calcarine fissure; 26: parieto-occipital fissure; 27: pons; 28: tectal
(quadrigeminal) plate; 29: medulla oblongata; 30: fourth ventricle; 31: cisterna magna;
32: interpeduncular cistern; 33: fornix; 34: mesencephalic aqueduct
292 11 Sagittal Planes Anterior Fontanelle

4 2

Fig. 11.5 (a) Second and fourth parasagittal planes through, respectively, right and
left lateral ventricles. (b–d) Ultrasound scans of fourth parasagittal planes through left
lateral ventricle. (b) Preterm neonate, GA 24+3 weeks, first postnatal day. (c) Preterm
neonate, GA 30+0 weeks, second postnatal day. (d) Full-term neonate. Note that with
proper positioning of the probe, the whole lateral ventricle and the ipsilateral cerebel-
lar hemisphere can be depicted in this plane.
11 Sagittal Planes Anterior Fontanelle 293

2
22
5
6 15
7 14

8 16
20
35
19a
23
3

Fig. 11.5 (continued)

294 11 Sagittal Planes Anterior Fontanelle

c
2

22
5
6 14
7
16
17 15
8
35
20
3

23
19a

Fig. 11.5 (continued)

11 Sagittal Planes Anterior Fontanelle 295

2
22
13
5 14
6
7 15
16
17 26
20
8
23
19a
3

Fig. 11.5 (continued) 2: frontal lobe; 3: skull; 5: frontal horn of lateral ventricle;
6: ­caudate nucleus; 7: basal ganglia; 8: temporal lobe; 13: cingulate sulcus; 14: body
of lateral ventricle; 15: choroid plexus; 16: thalamus; 17: parahippocampal gyrus;
19a: cerebellar hemisphere; 20: temporal horn of lateral ventricle; 22: parietal lobe;
23: occipital lobe; 26: parieto-occipital fissure; 35: occipital horn of lateral ventricle
296 11 Sagittal Planes Anterior Fontanelle

5 1

Fig. 11.6 (a) First and fifth parasagittal plane through, respectively, the right and left
insula. (b–d) Ultrasound scans of first (c and d) and fifth (b) parasagittal planes through,
respectively, right (c and d) and left (b) insula. (b) Preterm neonate, GA 25+1 weeks, first
postnatal day. (c) Preterm neonate, GA 30+0 weeks, second postnatal day. (d) Full-term
neonate, GA 40 weeks, postnatal day 8. Note the subtle, diffuse and homogeneous
echogenicity of the white matter in the preterm infants, a physiological phenomenon
at that age (see also Part I Chaps. 5 and 8).
11 Sagittal Planes Anterior Fontanelle 297

22

36

9 23

8 3

Fig. 11.6 (continued)

298 11 Sagittal Planes Anterior Fontanelle

22

36

9 23
8 3

Fig. 11.6 (continued)

11 Sagittal Planes Anterior Fontanelle 299

2 40
38

39
22
37

36

9 3

8 23

Fig. 11.6 (continued) 2: frontal lobe; 3: skull; 8: temporal lobe; 9: sylvian fissure;
22: parietal lobe; 23: occipital lobe; 36: insular area; 37: insular sulci; 38: central sulcus;
39: postcentral sulcus; 40: precentral sulcus
300 11 Sagittal Planes Anterior Fontanelle

5a 1a

Fig. 11.7 (a) Extreme parasagittal planes (1a and 5a) through, respectively, the right
and left insula. (b and c) Ultrasound scans of left extreme sagittal plane (5a).
(b) Preterm neonate, 28+2 weeks gestation, CUS on 7th postnatal day. (c) Full-term
neonate, GA 40 weeks, postnatal day 8.
11 Sagittal Planes Anterior Fontanelle 301

40

38
9 36

Fig. 11.7 (continued)

302 11 Sagittal Planes Anterior Fontanelle

40

39
36

38
9

Fig. 11.7 (continued) 3: skull; 9: sylvian fissure; 36: insular area; 38: central sulcus;
39: postcentral sulcus; 40: precentral sulcus
 12 Posterior Fontanelle

AF

PF

TW

MF

Fig. 12.1 The acoustic windows. AF anterior fontanelle, PF posterior fontanelle, TW

temporal window, MF mastoid (or posterolateral) fontanelle

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304 12 Posterior Fontanelle

Fig. 12.2 Probe positioning to obtain coronal views, using the posterior fontanelle as
the acoustic window

Fig. 12.3 Drawing of probe positioning to obtain coronal views, using the posterior
fontanelle as acoustic window
12 Posterior Fontanelle 305

Fig. 12.4 (a) Coronal plane through tentorium, cerebellum, occipital lobes and occipi-
tal horns of the lateral ventricles. (b–d) Ultrasound scans of coronal planes in preterm
infants (b, d born at 28 weeks gestation, CUS on fourth postnatal day; c born at 28+2
weeks gestation, CUS on seventh postnatal day), using the posterior fontanelle as the
acoustic window. (b) Superior coronal view through body of the lateral ventricles, pari-
etal lobe and brain stem. (c) Mid-coronal view through the occipital horns, occipital
lobes and cerebellum. (d) Inferior coronal view through the occipital lobes and
cerebellum.
306 12 Posterior Fontanelle

23

35
22
15

34 14
18

8
32

Fig. 12.4 (continued)

12 Posterior Fontanelle 307

35
23
25
21

19a 19b

Fig. 12.4 (continued)

308 12 Posterior Fontanelle

23
25

21

19b
19a

Fig. 12.4 (continued) 8: temporal lobe; 14: body of lateral ventricle; 15: choroid
plexus; 18: mesencephalon; 19a: cerebellar hemisphere; 19b: cerebellar vermis;
21: tentorial area; 22: parietal lobe; 23: occipital lobe; 25: calcarine fissure; 32: interpe-
duncular cistern; 34: mesencephalic aqueduct; 35: occipital horn of lateral ventricle
12 Posterior Fontanelle 309

Fig. 12.5 Probe positioning to obtain sagittal views, using the posterior fontanelle as
the acoustic window

Fig. 12.6 Drawing of probe positioning to obtain sagittal views, using the posterior
fontanelle as acoustic window
310 12 Posterior Fontanelle

Fig. 12.7 (a) Mid-sagittal view through parieto-occipital lobe, aqueduct, cerebellar
vermis, brain stem. (b) Ultrasound scan of midsagittal view using the posterior fonta-
nelle as acoustic window. Preterm infant born at 26+5 weeks GA, CUS day 2.
12 Posterior Fontanelle 311

26

25
28
19b
10
31
34
30
18
12 29

27

Fig. 12.7 (continued) 10: corpus callosum; 12: third ventricle; 18: mesencephalon;
19b: cerebellar vermis; 25: calcarine fissure; 26: parieto-occipital fissure; 27: pons;
28: tectal (quadrigeminal) plate; 29: medulla oblongata; 30: fourth ventricle;
31: cisterna magna; 34: mesencephalic aqueduct
312 12 Posterior Fontanelle

Fig. 12.8 (a) Parasagittal plane through occipital lobe and occipital horn and trigone
of the lateral ventricle and thalamus. (b) Ultrasound scan of parasagittal view through
the right lateral ventricle, using posterior fontanelle as acoustic window. Preterm
infant born at 26+5 weeks GA, CUS day 2. Note the bulky, echogenic choroid plexus
(normal finding).
12 Posterior Fontanelle 313

25
23
22
35

15
14
8
16 20

Fig. 12.8 (continued) 8: temporal lobe; 14: body of lateral ventricle; 15: choroid
plexus; 16: thalamus; 20: temporal horn of lateral ventricle; 22: parietal lobe; 23: occipi-
tal lobe; 25: calcarine fissure; 35: occipital horn of lateral ventricle
 13 Temporal Window

Fig. 13.1 Probe position for axial (or transverse) plane using temporal window

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([Link] contains supplementary material,
which is available to authorized users.

© Springer Nature Switzerland AG 2019 315

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
316 13 Temporal Window

Fig. 13.2 Drawing of probe positioning to obtain axial (or transverse) planes through
the temporal window
13 Temporal Window 317

Fig. 13.3 (a) Axial (or transverse) plane through the temporal lobes, upper cerebellum,
cerebral peduncles, aqueduct. (b and c) Ultrasound scans of transverse view, using
temporal window. Preterm neonate, GA 30+0 weeks, second postnatal day. (b) High
transverse view through third ventricle. (c) Lower transverse view through cerebellum.
(d) Very preterm infant, GA 24+6 weeks, postnatal day 1. Colour Doppler image of axial
plane through the temporal window, showing the circle of Willis (see also Chap. 3), Fig.
3.17 and Chap. 9).
318 13 Temporal Window

b
8
20 17
18
19b

32
34
12
41

Fig. 13.3 (continued)

13 Temporal Window 319

20
17

19
41
32 34

18

Fig. 13.3 (continued)

320 13 Temporal Window

d
8

20
42b
41
42a 18
19
42c

Fig. 13.3 (continued) 2: frontal lobe; 8: temporal lobe; 12: third ventricle; 17: parahip-
pocampal gyrus; 18: mesencephalon; 19: cerebellum; 19b: cerebellar vermis;
20: temporal horn of lateral ventricle; 32: interpeduncular cistern; 34: mesencephalic
aqueduct; 41: cerebral peduncle; 42: circle of Willis; 42a: anterior cerebral artery (ACA);
42b: middle cerebral artery (MCA); 42c: posterior cerebral artery (PCA)
 14 Mastoid Fontanelle

Fig. 14.1 Probe position to obtain coronal views, using the mastoid fontanelle as the
acoustic window

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([Link] contains supplementary material,
which is available to authorized users.

© Springer Nature Switzerland AG 2019 321

G. Meijler, S. J. Steggerda, Neonatal Cranial Ultrasonography,
[Link]
322 14 Mastoid Fontanelle

Fig. 14.2 Drawing of probe positioning to obtain coronal views, using the mastoid
fontanelle as the acoustic window
14 Mastoid Fontanelle 323

Fig. 14.3 (a) Coronal view through the temporal lobes, pons, fourth ventricle, cerebel-
lum, cisterna magna. (b–e) Ultrasound scans of coronal view, using the mastoid fonta-
nelle as the acoustic window. (b, c) Anterior coronal views, (d) and (e) posterior coronal
views. (b) Preterm neonate, GA 25+3 weeks, first postnatal day. (d) Preterm neonate, GA
30+0 weeks, 2nd postnatal day. (c, e) Full-term neonate. Note the impressive growth
and maturation of the cerebellum during the neonatal period.
324 14 Mastoid Fontanelle

19a
31
30 19b
18
21
20

Fig. 14.3 (continued)

14 Mastoid Fontanelle 325

44

19a
19b
31
30 43
18

Fig. 14.3 (continued)

326 14 Mastoid Fontanelle

d
8

14 19a
15
31
19b

21

3
22

Fig. 14.3 (continued)

14 Mastoid Fontanelle 327

44

35
31
19b

21
19a

Fig. 14.3 (continued) 3: skull; 8: temporal lobe; 14: body of lateral ventricle;
15: choroid plexus; 18: mesencephalon; 19a: cerebellar hemisphere; 19b: cerebellar
vermis; 20: temporal horn of lateral ventricle; 21: tentorial area; 22: parietal lobe;
30: fourth ventricle; 31: cisterna magna; 35: occipital horn of lateral ventricle;
43: foramen of Magendie; 44: cerebellar folia
328 14 Mastoid Fontanelle

Fig. 14.4 Probe positioning to obtain axial (or transverse) views, using the mastoid
fontanelle as the acoustic window
14 Mastoid Fontanelle 329

10º

Fig. 14.5 Drawing of probe positioning to obtain axial planes, using the mastoid fon-
tanelle as acoustic window
330 14 Mastoid Fontanelle

Fig. 14.6 (a) Axial (or transverse) plane through the temporal lobes, pons, fourth ven-
tricle, cerebellum, cisterna magna seen from below. (b–f) Ultrasound scans of axial
views, using the mastoid fontanelle as the acoustic window. (b, c) Superior axial view,
(d, e) mid-axial view, (f, g) inferior axial view. (b, d) Preterm neonate, GA 25+3 weeks,
first postnatal day. (f) Preterm neonate, GA 30+0 weeks, 1st postnatal day. (c, e, g) Full-
term neonates. Note the ongoing maturation of the cerebellum and the fissures cross-
ing over the complete cerebellar surface in the full-term neonates.
14 Mastoid Fontanelle 331

19
41 18
32

8 3

Fig. 14.6 (continued)

332 14 Mastoid Fontanelle

19

18

Fig. 14.6 (continued)

14 Mastoid Fontanelle 333

20 19a
31
19b
27
30

Fig. 14.6 (continued)

334 14 Mastoid Fontanelle

44

19a

31
27 19b
30

Fig. 14.6 (continued)

14 Mastoid Fontanelle 335

19a

31
43
19b
27

Fig. 14.6 (continued)

336 14 Mastoid Fontanelle

44
19a

31
19b
29

Fig. 14.6 (continued) 3: skull; 8: temporal lobe; 18: mesencephalon; 19: cerebellum;
19a: cerebellar hemisphere; 19b: cerebellar vermis; 20: temporal horn of lateral ventri-
cle; 27: pons; 29: medulla oblongata; 30: fourth ventricle; 31: cisterna magna; 32: inter-
peduncular cistern; 41: cerebral peduncle; 43: foramen of Magendie; 44: cerebellar folia