How to get the most from axial views of the fetal brain: applying the principles of neurosonography to screening examination of the supratentorial central nervous system

Central nervous system (CNS) anomalies are among the most common malformations diagnosed prenatally. In clinical practice, the second-trimester screening assessment for fetal CNS anomalies is accomplished through evaluation of the axial views of the fetal brain. However, if an anomaly is suspected, an extended multiplanar assessment of the fetal brain (‘fetal neurosonography’) should be performed by an expert. This includes evaluation of the sagittal, parasagittal and coronal views of the brain, which allows visualization of structures that cannot be identified in the axial views, such as the corpus callosum, the cerebellar vermis and the hemisphere proximal to the transducer. Neurosonography should also be performed in cases with a family history of inheritable CNS malformations or a previous pregnancy affected by a fetal CNS anomaly, and in the presence of congenital heart disease or fetal infection1. While an objective description of the CNS anatomy is only possible using neurosonography, the anatomical relationship between the different supratentorial intracranial structures can be described using the axial planes of the brain, and strong suspicion of an anomaly may be raised from examination of these imaging planes. Herein, we propose a step-by-step approach to identifying the most common supratentorial anomalies from the axial views of the fetal brain, applying the principles of neurosonography to these imaging planes. This approach is not intended to replace multiplanar assessment of the fetal brain, which is the only way to diagnose CNS anomalies, but rather aims to improve the ability to confirm normal brain anatomy during routine screening of the fetal CNS. If a brain anomaly is suspected or when there is an increased risk for anomalies, neurosonography should be performed (Figure S1c–e)2. Our step-by-step approach provides a detailed anatomical description of the supratentorial fetal brain, to assist in detection of the most common and severe CNS malformations using the axial views of the fetal brain. The rationale behind this is that some of the most common supratentorial anomalies are associated with a unique rearrangement of the intracranial structures, which can be suspected even from the axial views of the fetal brain. Our approach is based on a series of simple clinical questions that should be applied during a second-trimester screening assessment of the fetal brain (Figure 1). Anatomy. The calvarium is composed of multiple bones: two frontal bones, two parietal bones, two temporal bones, the upper part of the occipital bone and the sphenoid wings. Each bone is separated from the others by membranous spaces called sutures. The major sutures are the metopic suture, located between the frontal bones, the sagittal suture, located between the parietal bones, the coronal suture that separates the frontal bones from the parietal bones, and the lambdoid suture that separates the parietal bones from the occipital bones (Figure 2a). The posterior borders of the parietal bones are separated from the upper border of the occipital bones by the lambdoid sutures. The irregular spaces connected with the membranes of the sutures are the fontanelles; the largest is the anterior fontanelle, located at the intersection between the sagittal and coronal sutures3. Ultrasound appearance. At ultrasound examination, the calvarium has an oval shape, interrupted at the level of the sutures, which appear as anechoic lines interrupting the continuity of the cranial bones (Figure 2b,c). Calvarium is absent. Absence of the calvarium is typical of acrania–exencephaly–anencephaly sequence, which may be identified at the 11–13-week scan4-6. An abnormal fetal head contour may be associated with fetal anomalies, oligohydramnios or breech presentation, but can also represent a normal variant4. Differential diagnosis requires multiorgan assessment, neurosonography and echocardiography. Calvarium is present, but there is a defect in the cranial bone. This defect is defined as cephalocele, and it is usually located in the occipital bone. It appears as a sac-like structure, commonly covered by skin, protruding from the fetal head. The contents of the cephalocele sac connect with the intracranial portion of the brain through the cranial defect (Figure 2d)7. Calvarium is present, but the cranial contour is abnormal, with flattened appearance of the frontal bone. Typical of neural tube defects (NTD), this is known as the ‘lemon sign’. In this anomaly, the frontal bones lose their convex contour and appear scalloped inwards (Figure 2e). The pathophysiology of this structural anomaly in the head of fetuses with NTD has not been fully elucidated but seems to be associated with reduced intracranial pressure following herniation of the brainstem through the foramen magnum. Another imaging sign associated with NTDs in the axial view of the fetal brain is the ‘banana sign’, which is a result of the abnormal configuration of the cerebellum associated with obliterated cisterna magna1, 8. Calvarium is present, but the cranial contour is abnormal, with flattening of the occiput and pointing of the frontal bones. Also known as ‘strawberry-shaped’ head (trigonocephaly), this is a sign of chromosomal anomaly, mainly trisomy 18 (Edward's syndrome) (Figure 2f), or skeletal dysplasia, mainly thanatophoric dysplasia9, 10. Trisomy 18 is associated with multiorgan fetal anomalies and fetal growth restriction, while skeletal dysplasia presents with long bones that are very short, thoracic hypoplasia, relative cardiomegaly and systemic anomalies. Only severe skeletal dysplasia can be suspected at the time of the anomaly scan. Calvarium is present, but the cranial contour is abnormal, with flattening of the occiput, widened cranium and bulging forehead. Also known as brachycephaly, this may be a sign of Down syndrome or other trisomies (Figure 2g), or may represent a normal familial variant. Similarly, some rare syndromic conditions, such as Apert, Crouzon, Carpenter and Pfeiffer syndromes, are also associated with this abnormal contour of the calvarium, together with facial and limb abnormalities. However, when no other anomaly is present, this head shape is likely to represent a benign finding11, 12. Calvarium is present, but the cranial contour is abnormal, and the anechoic cranial sutures cannot be visualized. This is a sign of craniosynostosis, a heterogeneous group of anomalies characterized by premature closure of the cranial sutures to an abnormal shape of the fetal head (Figure The most common of cranial anomaly is defined as a head shape from to It is also in skeletal dysplasia, but may represent a familial when there are no associated Anatomy. The is a that separates the two (Figure the a of the is Ultrasound appearance. The can be in the axial planes from the of pregnancy as a from the frontal bone to the occipital bone of the fetal the (Figure is absent. Absence of the is a common sign of an anomaly commonly diagnosed in the of The of is commonly in the frontal ultrasound of in the axial view of the fetal brain are the presence of a of the and (Figure is in of the in is a sign of severe and is associated with severe of the system (Figure It is to from of the in fetuses with severe from to the increased Typical ultrasound of severe associated with of the anterior of the abnormal between the two in the and but separated the and the corpus are usually present, but to in fetuses with the of in the most anterior part of the frontal with the is and there are commonly associated facial mainly severe is interrupted by anechoic This sign may be associated with the presence of an or anomalies. presents as an irregular commonly located the (Figure in the frontal part of the brain are commonly associated with anomalies, mainly of the corpus anechoic posterior to the the presence of a a benign associated with normal (Figure An of the supratentorial anomalies is of which appears as an anechoic on the axial view of the fetal brain, with the by (Figure anechoic in the posterior part of the brain the presence of (Figure this is associated with a or of the The presence of an the may a of the is present, but of the can be associated with anomalies, brain a or of the anterior part of the with normal brain and in the of intracranial or has been associated with a of CNS anomalies, malformations of anomalies and and should detailed multiplanar assessment of the fetal is present, but are of the is commonly this may represent an imaging usually to of the imaging it may represent a common associated with different CNS anomalies should a multiplanar assessment of the fetal brain. in the fetal brain may be a of an intracranial such as a brain which appears on imaging as a with and such as which is characterized by a of or part of a from increased or of an axial view of the fetal brain, presents as in the with the affected and is commonly associated with and brain anatomy (Figure Anatomy. The is a or located in the anterior of the brain, in the and between the anterior portion of the and the of the (Figure The is with a of from the through the and it not with the The is part of the system and is in the brain. The of the are by the and of the by the of the and the by the anterior and the of the and by the of the The may be connected to a posterior the Ultrasound appearance. The can be identified on ultrasound from to of in the the of the the visualization of the from the of pregnancy using the appears as an anechoic or and appear as two lines (Figure The anterior of the the and the which can be as a to the The of the at the time of the anomaly has been to be in the of the fetal brain, and is The should not be with the of the which are located to the as lines through the part of the anterior portion of the brain, and not (Figure of a or not that the and of the are is absent. Absence of the is the most common sign of (Figure of this diagnosis is possible only on neurosonography, the of visualization of the in a sagittal view of the brain (Figure imaging typical of in an axial view of the fetal brain widened (Figure abnormal of the frontal from the and appearance of the is and but with a This may be a sign of (Figure and is the only sign of this anomaly in an axial view of the fetal brain, as the common of abnormal of the frontal and are not usually in cases with of requires a sagittal view of the fetal brain, the of a portion of the the part or the or presence of an (Figure is and or in shape, but is or of the but with a appearance is defined as obliterated (Figure This described only It may represent a normal with visualization of anechoic in the or in with different anomalies, of the and (Figure In a series of fetuses with obliterated the normal in of while there associated anomalies identified at ultrasound or mainly the and in of of the and of the when an obliterated is is to it is assessment of cannot be performed at the time of the anomaly and requires a in the can be associated with the presence of a is present, anechoic and or in shape, but is no on to a for the in the and of pregnancy been using that the of at of is However, a of to the as (Figure has been in with chromosomal anomalies, with these anomalies when it is as an is risk of has also been in with a is not as an for multiplanar brain assessment in the it seems to neurosonography in fetuses with this is present, anechoic and or in shape, but At of the for is may be associated with when the system is to in the of for at the of or the system and the and anatomy is can be a normal and should not be as an for neurosonography (Figure Anatomy. The frontal are of the the frontal of the brain (Figure the of the and are structures composed of a an and the temporal and occipital The of frontal is by the most anterior part of the and the is by the head of the The of is to the of the In the of the brain, the frontal the time of the anomaly the can be only in the portion of the and the portion of the and the of the and is in the proximal part of the frontal anterior to the of Ultrasound appearance. In the axial of the fetal brain, the frontal appear as two anechoic or structures (Figure The of frontal is but the of the while the the The appear as structures on of the frontal is not performed during the second-trimester screening ultrasound examination of the fetal brain, an anomaly, mainly is The for the frontal their at the from to to the and the defined as the from the of the of the frontal to the of the The two frontal in in of a that is of clinical but is likely if it in are and but from the This is a sign unique to (Figure However, of can be accomplished only in a sagittal view of the fetal brain, by of the of the (Figure The of the a unique appearance at the level of the anterior in an axial view of the fetal this can also be in the coronal view (Figure The most common sign of in the axial views of the brain is of the However, an if present, or the of the may be for the In most cases of which are to the an which to the and the in the anterior part of the frontal In this the frontal are from the and their a appearance by the in axial and coronal views (Figure can also with the presence of an located in the proximal part of the In this the frontal are from the the diagnosis of (Figure are and but appear to be with the of between the of the frontal and the of the with of these structures, of dysplasia or (Figure The diagnosis between these is possible only at neurosonography, but requires as the imaging of these anomalies may only in or of the and a appearance of the frontal and the presence of while the presence of is typical of (Figure there is no imaging of these the diagnosis is likely to be However, this cannot be and is associated with a of diagnosis of are anechoic and from the but of the normal of the frontal irregular or when the portion appears the when associated with may represent a common sign of malformations commonly with other anomalies, and abnormal (Figure are anechoic and from the but is no to the frontal as and this sign on assessment (Figure of the frontal may represent a normal or be associated with when in the frontal is should be to occipital and to the and are and from the but the of the not the frontal the presence of the at the level of the frontal is a normal sign and is commonly associated with intracranial this may represent the sign of a rare (Figure frontal or the of the can be associated with or Anatomy. The is a located in the and the part of the system (Figure It with the the of and with the the The is or in shape and has a and a The is by the and while the is of the neural the and the The is a that is from the and which to the The and the of the The upper portion of is the of the anterior of the while the and the the part of the The anterior of the is by the and the posterior is composed from to the the and the are the as a of the of the the in the between the of the and the of the the the and the Ultrasound appearance. The can be during ultrasound from of in the axial view of the fetal brain. In the at the time of the routine fetal anomaly it appears as a anechoic on in located between the the (Figure The of the is not in an axial view of the fetal brain. The anatomy of the is in the sagittal view of the fetal brain, of anatomical (Figure of the can in between and is It is that a in at should detailed assessment of the fetal brain using a multiplanar may represent a sign of (Figure In to there is also of the portion of the and of the posterior the cisterna in this in a axial view of the fetal brain, the posterior portion of the the of the fetal brain. is and has the a rare this may represent a sign of severe intracranial The are by in the which can to (Figure In to the can also appear but commonly has in the or is absent. Absence of the is a common sign of (Figure this anomaly is commonly diagnosed in the of ultrasound of in the axial view of the fetal brain are the presence of a and and (Figure with frontal This may However, diagnosis between and is and requires is of the is a common sign of However, this is identified in a coronal view of the fetal brain (Figure imaging typical of that can be in an axial view of the fetal brain of visualization of the widened of the normal of the frontal and appearance of the occipital and Anatomy. The occipital of the are or structures which from the and the occipital (Figure The commonly the portion of the posterior but not Ultrasound appearance. of the occipital of the is a part of the screening assessment of the CNS during the of In the axial the and of the occipital appear as two lines that are but not to the and the which appears anechoic (Figure The of the the of the which appears as a structure, the and is in with the and in some normal cases a of may be between the and the The part of the occipital appear as anechoic structures are with the the are at the level of the of the the by the The normal to normal is between the two is to represent a normal if the is the normal of the is a but is This of in the axial view of the brain with normal frontal and while visualization of the and may be in cases of or severe (Figure In the the but not the portion of the occipital and is is normal in of fetuses with of the is normal or increased in a but are and This can be a sign of or In the axial view of the fetal brain, in the of the are which is a sign of (Figure are also present, as the (Figure In intracranial the can be normal or and there are in the as as an irregular of the and as (Figure and of the is normal or increased in a but has or in This can be a sign of (Figure and or of to the presence of (Figure In intracranial the can be normal or and there are as as as in the and irregular of the The should be from which are associated with (Figure and and from to the can to of the is normal or increased in anechoic and with a but has a This known as is characterized by and of the and the occipital and of the temporal It is a sign which can be in CNS anomalies, it is associated with (Figure Anatomy. In the or is the of the brain to the composed of of which and to their the and (Figure In the and of the which connect the with the in the of and it is not This the of the brain different from that in it is mainly by a which by and the of the in the of with of and which the part of the the from the and in a which allows and the of the brain. and to the of the during this can to the of which commonly with or clinical for the of to The of the brain is to which mainly to the of The most common congenital such as and a for the fetal Ultrasound appearance. In the in the axial the presents as a and anechoic the with a the between the the brain and the calvarium (Figure of the is in the occipital the frontal of the of the presence of the located to the of the frontal of the appearance of the may suspicion of fetal CNS anomalies that and and or in the mainly in the occipital of the This may be a sign of or located mainly the posterior when associated with may be a sign of The presence of may also be a sign of intracranial and is associated with and and irregular borders (Figure of protruding the of the occipital of the The presence of of protruding the of the posterior is a sign of (Figure is a in which the to from the the and as that the is associated with a risk of and commonly presents with heterogeneous clinical such as or in the frontal are usually also known as or (Figure are usually located in the or of the frontal of the are not by and are to following or of the (Figure are commonly in the may be identified in the a can be associated with fetal growth restriction, and structural or chromosomal anomalies. result from in the and are associated with a risk of (Figure The diagnosis between these two by based on their to the frontal of the and it is accomplished mainly by a coronal view of the fetal brain. usually the of the (Figure while are this Anatomy. the of in the and and of the fetal is in the of pregnancy at the time of the routine anomaly scan. The that can be identified in the in hemisphere the also known as the the the and the The is the on the of and is by the between the the temporal and the (Figure The is an located in the posterior part of the of hemisphere and the between the occipital and parietal (Figure The is located on the of occipital the of and the two it the while it the occipital The is located on the of a the border of the from anterior to posterior and it from the Ultrasound assessment of the at the time of the routine second-trimester anomaly has not been fully of the may represent an sign of abnormal the of this sign in these is associated or anomalies. and the of appearance of the that only the and can be identified in the axial view of the fetal brain at the time of the routine anomaly of the in the axial view of the fetal brain described by and in a that the and characterized by the presence of anatomical the of the the and the cisterna (Figure and has been in the axial and parasagittal views of the brain by and and by the and between the The can be the of the occipital of the in a axial view of the fetal brain as a in the which a by of (Figure of the includes mainly which can be by a from the of the to the contour of the or to the level of the The can be identified in the axial view of the fetal brain (Figure as a to the anterior to the and the while it is commonly in a coronal view (Figure the can be identified mainly by a view of the brain at the level of the part of the posterior of the of the is normal in the fetal is or for and to been in the there is no on to an abnormal on on axial views of the fetal or appearance has been in of cases of diagnosed However, that the appearance of the at the time of the second-trimester not assessment for mainly cases with associated the of or of this when in is appearance of the has been defined by some as the of a or to the In view of the in and the of assessment, routine of the during the second-trimester is not and should on and on of appearance (Figure in which the cannot be or in which a is should be for neurosonography, in cases of of the and normal may not be structures may be the are commonly benign and with a risk of or (Figure is or evaluation of the to is not at the time of the routine anomaly as the of this during the is commonly it likely that routine assessment be associated with a of of brain However, it seems to for neurosonography fetuses in which of the two is not or when are as in some cases this can be associated with a brain anomaly (Figure evaluation of the is not as this commonly in the and it cannot be identified at the time of the routine second-trimester anomaly Anatomy. of fetal in the and of pregnancy and and in the in the and the of the a This in with the previous that the are located to the of the at of and includes of a of and which from and of from of in between of and of The of the located the the of are for the of the neural the of the and of multiple among the at of the is by Ultrasound assessment of normal brain and has been using coronal views of the fetal brain. This allows visualization of the and which are most in the and of The appears as a anechoic the and is separated from the by a The located the appears the The is as a the frontal of the pregnancy visualization of the brain but is accomplished mainly in coronal views using in axial views of the fetal brain, are not and the brain appears or has or This imaging sign may be associated with different supratentorial anomalies, anomalies from and intracranial and are associated with anomalies and while intracranial is associated with and the brain of the may the presence of brain is or or This may be associated with intracranial or are commonly located in the while is to the frontal of the can also represent the of intracranial anechoic the to the (Figure this anomaly is identified in a parasagittal or coronal view of the brain (Figure of of for the is not to this as no or in this and axial views of the fetal brain for screening assessment of nervous system (CNS) anomalies, as by the of Ultrasound in and sagittal parasagittal and coronal views of the fetal brain for neurosonography, as by Ultrasound imaging of the fetal brain different clinical characterized by anomalies suspected in the axial view of the fetal brain. of on axial view the of the which appear as in the anterior part of the brain. axial view of a a sagittal view of the brain, in which the corpus appears with a but not is and or in shape, but is with a normal corpus on view of the fetal brain at the level of the frontal their with the view presence of the corpus In the coronal view of the fetal brain the frontal appears with a in the which appears as an anechoic the frontal with the of the brain and the ultrasound of view of the fetal brain in a with of the frontal and and parasagittal views of the brain in a with which appear as a the there is a the proximal part of the occipital of the and to the frontal to view of the fetal brain an between the posterior part of the occipital and the of the brain, The is not for the or of by the should be to the for the