Neonatal cranial ultrasonography

NEONATAL CRANIAL ULTRASONOGRAPHY

ABSTRACT.-We trace the evolution of pediatric cranial from its inception to the present. Technical considerations pler imaging are discussed. Scanning techniques and a sonographic landmarks of normal anatomy are presented. of these landmarks will facilitate screening examinations. We then present clinical and screening indications sonography in the neonate, emphasizing the pathogenesis fication of intracranial hemorrhage and porencephaly. scription of inflammatory lesions and their sonographic and a review of cystic and solid lesions completes the cranial sonography in the neonate.

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sonography and Dopreview of the Knowledge for cranial and classiFinally a deappearances discussion of

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Johan G. Blickman, M.D. is Assistant Professor of Radiology School and Radiologist in the Pediatric Radiology Division General Hospital.

Diego Jaramillo, and a Radiologist Hospital.

at Harvard Medical of the Massachusetts

M.D. is an Instructor in Radiology at Harvard Medical in the Pediatric Radiology Division at Massachusetts

School General

Robert H. Cleveland, M.D. is an Associate Professor of Radiology at Harvard Medical School and is Director of the Pediatric Radiology Division of the Massachusetts General Hospital. Cum

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NEONATAL CRANIAL ULTRASONOGRAPHY

HISTORY Attempts made to locate the sunken liner Titanic represent the earliest recorded use of ultrasound to find submerged objects. During World War II, the British applied echosounding used in testing industrial metals to track German submarines in the Atlantic, employing high frequency sound waves conveyed through ocean water as a medium. This technique was called SONAR (Sound Navigation and Ranging). Medical applications of SONAR were attempted before World War II, but only became feasible when advanced circuitry enabled a single transducer to emit sound waves, receive their echoes, and transform these echoes into an electrical pulse by means of the piezoelectric properties of the crystal in the transducer.“’ These piezoelectric properties, described below had already been discovered in 1880 by Pierre and Jacques Curie. Military sonar uses a technique called A mode (or amplitude modulation). Vertical spikes are created along a baseline, the height of the spike being related to amplitude of the echo. Since the height of the spike from the baseline is proportionate to the distance of the object from the transducer face, the distance from the surface hunter ship to submarines can be computed. B mode, or two-dimensional sonography, was developed in the middle 195Os, again for military use. In early attempts at medical use the bomb turret of a B29 bomber was tilled with water, and the patient was immersed in it. The images were poor, but in the early 1960s images from animal Curr

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studies obtained by this water-immersion scanning technique were compared with anatomical specimens. This technique was, however, cumbersome, and artifacts were numerous. For example, ultrasound waves do not readily penetrate an adult skull, and ultrasound is, therefore, of limited value in delineating intracranial structures if the calvarium is intact.3’ 4 In the early 197Os, it became obvious that very premature neonates (<32 weeks gestation) could be kept alive, but were at high risk for intracranial abnormalities such as hemorrhage and posthemorrhagic complications.5-8 Computed tomography (CT) scanning was the established method of cranial imaging at this time,” ’ but, as with the static B mode and water immersion techniques, it was nearly impossible to employ CT routinely for patients in the neonatal intensive care unit (NICU). Bedside NICU imaging began when real-time sector scanning became available through the manufacture of lightweight easily portable units.l’ In the early 198Os, a number of reports described real-time scanning through the anterior fontanel and assessed the diagnostic usefulness of portable NICU ultrasound scanning.11-15

TECHNICAL

CONSIDERATIONS

Real-time scanning through the anterior fontanel can be performed by a sector scanhead or a linear array scanhead, which employ either an oscillating single crystal or an array of crystalsl” l7 96

These crystals can transform electrical iIT@SeS into sound waves, then receive the reflected waves and transform them back into electrical impulses. This property is called the piezoelectric effect. It belongs to quartz and some ceramics and enables them to be used as ultrasound scanheads. Sector scanners are the most commonly used scanners for cranial ultrasonography today. In mechanical sector scanning, a single transducer oscillates at high speed, producing a wedge-shaped image. The ultrasound image consists of the different amplitudes of the sound waves reflected from the different tissues, resulting in a gray scale that differentiates structures. The image so created can be manipulated by the operator. The depth of focus of the beam can be varied to bring different planes into optimal view. The digital scan converter, developed from the analog converter, serves as a memory for the images thus acquired, allowing further enhancement through digital preprocesssing and postprocessing. In linear array transducers, piezoelectric crystals are aligned in series. This arrangement provides the best resolution in the near field and is optimal for detecting lesions in the convexity of the brain, for example, subdural hygromas. Far-field imaging

is also enhanced by series alignment. However, linear array real-time equipment employs a large transducer head which may be difficult to use in a small fontanel or on a curved cranial surface, both of which are frequently present in the same premature child. Phased array scanners sweep the ultrasonic beam electronically through the scanned plane using a time-delay method that allows further improvement in resolution of the gray scale. These arrays of piezoelectric crystals can also be arranged in a curve in order to improve contact with a small fontanel. Resolution will therefore be further improved, facilitating visualization of the lateral portions of the intracranial contents. The matrix camera with six images per film is most frequently used for hard copy records and provides a standardized set of images in both the sagittal and coronal planes. The recently developed laser camera records all 12 images on one film. Video recording of the entire examination is especially useful if technologists or residents perform the study or if complex pathology is noted that needs further study in addition to the hard copy record. DOPPLER

IMAGING

As ultrasonic examination of the cranium in children progressed from being the one-dimensional (A model to the two-dimensional (B mode), visualization of blood flow progressed from the early nineteenth-century observation of the Doppler effect to the introduction of continuous and pulsed wave technology in the early SOS.~~-~’ Medical duplex scanning is based on pulsed Doppler, not on continuous Doppler. This technique permits examination of the intracranial vessels, in particular the circle of Willis and the pericallosal arteries. It has been shown to have diagnostic value, particularly in assessing conditions such as brain death” and complications of extracorporeal membrane oxygenation.23 Color flow Doppler is a further refinement that will find increased use in the NICUZ4’ ” (Fig 11. Studies have shown the value of color flow mapping in visualizing blood flow in small vessels. This technique may also permit evaluation of vascular&y in pediatric tumors and in the follow-up of patients receiving extracorporeal membrane oxygenation. SCANNING

TECHNIQUES

FIG 1. Color flow Doppler images of the coronal view; B, sagittal view. 96

infant’s

normal

circulation.

A,

As the premature infant is in essence a displaced fetus, the ambient temperature and envicurr

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ronment of the NICU should be as much like the uterus as possible. Interference with this state needs to be brief and targeted, and personnel should observe proper procedums.26 Use of gowns and gloves is recommended, and the portable ultrasound machinery should be kept clean. The transducers should be cleaned with alcohol between procedures and the -coupling agent (gel) should be heated to body temperature. The infant should be disturbed as little as possible, preferably being left in the isolette. If the child must be removed from the isolette, heating lamps should be in position. Sedation and immobilization are not necessary. It is essential, however, that the procedure be done in consultation with the nursing staff. Transducer frequency and focal length have become relatively standard. A 5 MHz transducer with medium focal length is generally satisfactory for most infants; however, a 7.5 MHz transducer is useful in the tiny premature. Often the relatively short focal length is ideal in this situation. Multifrequency scan heads have recently been introduced; these are most useful when several infants need to be imaged consecutively. Variable focal zones are also available with this probe. There are no contraindications to neonatal cranial ultrasonographic examination as currently practiced.27 It is difficult to evaluate the safety of diagnostic ultrasound because studies of safety have employed continuous wave ultrasound, whereas diagnostic ultrasound uses pulsed waves. The applicability of results is unclear. The American Institute of Ultrasound in Medicine has stated that the “low megahertz frequency range in which diagnostic ultrasound is employed reveals no significant biological effects in mammalian tissues that have been exposed to intensities below 100 mW/cm2.“28 As diagnostic ultrasound has been in use for over 2.5 years and no adverse biological effects on patients or instrument operators have been noted, it is assumed that the benefit to the patient far outweighs any potential risk and that examinations are harmless as long as the above limits are observed.‘” This observation may not apply to intrauterine evaluations by Doppler: A recent manufacturer’s communication suggested that heat production during intrauterine Doppler evaluation of flow may be harmful.“” The results of any ultrasonographic evaluation are highly operator dependent, which means that these rules need not be a limitation to trained sonographers. Cranial sonography should not, however, be employed indiscriminately in all premature infants. A protocol for screening and follow-up, as well as a clear understanding of indicaCurr

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FIG 2. Location

of the six coronal

planes

tions, is necessary. These points will be discussed after a review of the normal anatomy.

NORMAL

ANATOMY

The usual screening sequence consists of six images in the coronal plane (Fig 2) and six images in the sagittal plane (Fig 3). In the coronal plane, the transducer is angled from anterior to posterior in six positions. In the sagittal plane, the midline is imaged twice; then each hemisphere is imaged twice through the lateral ventricles. Realtime evaluation of the brain parenchyma from the lateral extreme of one hemisphere to the other should also be performed. The following suggested landmarks for coronal and sagittal imaging are not absolute. They are merely intended as references so that important structures can be noted and abnormal images can be correctly iden-

FIG 3. Location

of the sagittal

planes

superimposed

on the Infant’s

head.

FIG 4. A, location

of section

1; B, ultrasound

image:

C, outstanding

landmarks:

orbits,

interhemisphenc

fissure.

tified. The twelve sections that will be demonstrated are in our experience, most effective for screening the intracranial structures in premature neonates.

appearance denotes dilatation. Increased size of the interhemispheric fissure may indicate atrophy or subdural/subarachnoid fluid collections.

CORONAL

SECTION

IMAGING

SECTION I The most anterior section of the coronal plane can be identified from the gently undulating symmetric curve of the anterior fossa bisected in the midline by the falx cerebri (Fig 4). The frontal lobes on either side should be featureless, and no ventricular volume should be visible. One can see the posterior aspects of the orbital cones and occasionally the optic nerve running through the orbital cone. The echogenic structures of the ethmoid sinuses can be visualized inferior to the falx cerebri. One should not normally visualize ventricles in this anterior location (frontal horns), as such an

II

The second plane uses the Circle of Willis as its landmark inferiorly (Fig 5). The bilateral origin of the middle cerebral artery at the bifurcation of the supraclinoid internal carotid artery makes this complex resemble an anvil. It has also been described as a &pointed star or a bull’s head with the middle cerebral arteries being the horns and the sphenoid sinus echo complex, the head. The thalami are encompassed within the horns of this bull’s head. A slightly more echolucent area adjacent to the ventricles represents the subependymal germinal matrix. Superiorly between the two ventricles, two horizontal hard echoes delineate the anterior portion of the corpus callosum. The paired pericallosal arteries produce the superior

FIG 5. A, location 98

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C, outstanding

landmarks:

anvil,

bull’s

horns,

Spointed Curr

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The falx cerebri in the interhemispheric fissure should be easily identified. Fluid can often be seen in the interhemispheric fissure and along the convexity. This may be benign subdural collection of infancy, which consists of CSF and is a useful marker of the falx cerebri (Fig 6). It is difficult to distinguish germinal matrix hemorrhage from the most anterior portion of choroid plexus in the roof of the third ventricle protruding through the foramen of Monro. Germinal matrix hemorrhage is more easily assessed in the sagittal plane, but an asymmetric appearance will occasionally suggest that germinal matrix hemorrhage has occurred. In short, there should not be any choroid plexus anterior to the foramen of Monro; any hyperechoic area anterior to this structure represents pathology.

SECTION FIG 6. Benign

subdural

collection

of infancy.

echo, above the corpus callosum, and the inferior echo, below the corpus callosum, represents the roof of the cavum septum pellucidi. The slit-like frontal horns extend at an acute angle (<30”) outward from the midline with respect to the corpus callosum. These paramedian structures may be either slit-like or slightly distended by CSF in this location; the latter appearance permits easier identification. One may occasionally detect the putamen and globus pallidus, the echo texture of the latter being somewhat greater. The internal capsule can be identified as a band of decreased echo texture separating the globus pallidus and the putamen fi-om the thalamus. The external capsule is lateral to these structures,

III

This section is identified inferiorly by a pulsating vertical structure, the basilar artery, midline within the interpeduncular cistern (Fig 7). The boundaries of the interpeduncular cistern are formed by the choroidal fissures with the cerebral peduncles on each side. The middle cerebral artery pulsates within the Sylvian fissures and resembles a Y turned on its side. Lateral to the basal ganglia, the internal capsule can again be identified as a symmetrical structure. The third ventricle can be identified in the midline immediately caudad to the septum pellucidum. These midline structures are visible in 90% to 95% of all patients. The frontal horns should still be slit-like. The interhemispheric fissure may occasionally be visible on this section. It is unusual to visualize the temporal horns in this section; such visualization usually represents abnormality. Subdural collections may occasion-

FIG 7. A, location

Of

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of sectton

III, C,

outstanding landmarks:

interpeduncular cistern, third ventricle, 99

FIG 8. A, anatomic bellar

location

of section

IV; B, sonographic

image;

C, outstanding

ally be seen in this plane, Sylvian fissure.

SECTION

either laterally

or in the

ZV

The distinguishing feature of the fourth section is the tentorium cerebelli (Fig 8). Inferior to this tent-shaped structure the cerebellar vermis can be seen as a highly echogenic structure due to the high number of crossing fibers that create ultrasonic interfaces. The cerebellar hemispheres will be seen as relatively hyperechogenic structures bilaterally. In particular, the structure immediately superior to the apex of the tent, the quadrigeminal plate may resemble the top tier of a Christmas tree. Sylvian fissures are again seen bilaterally. Occasionally the choroid plexus may be seen adjacent to the region of the caudothalamic groove of the basal ganglia or slightly posterior to it. Infratentorial lesions are frequently well visualized in this plane (fourth ventricle).

FIG 9. A, locatlon 109

landmarks:

quadrigeminal

plate

cistern

“Christmas”

tree,

cere-

vermis

of section

V; B, sonographlc

image;

C, outstanding

SECTION

V

The outstanding feature of the fifth section is the “moustache” view, which is formed by the glomus of the choroid plexus in the atrium or trigone of the lateral ventricle (Fig 91. There should be no ventricle visible around the choroid plexus at this point, but a tiny amount of CSF can sometimes be seen, especially on the dependent side. Radiating laterally from these structures is an echogenic blush containing the highly echogenic fibers of the optic tracts. Occasionally the splenium of the corpus callosum can be seen as a horizontal structure in the midline, the Sylvian fissures at this point having blended into normal cortical markings.

SECTION

VI

This section has as its landmark the centrum semiovale, which at this level consists of the decussation of fibers of the optic tract that are visible

landmarks:

glomus

of the choroid

plexus Cum

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as a blush located symmetrically on either side of the interhemispheric fissure (Fig 10). No other distinguishing landmarks are seen on this final section in the coronal plane. Any asymmetry should suggest periventricular leukomalacia.

resent the best reference points for obtaining images of the lateral sections of the cerebral hemispheres (Fig 11,C).

THE SAGWIXL

IMAGING

The sagittal images constitute the second portion of the screening examination. There are several ways of screening in the sagittal plane, but images should include two midline sections, and two sections each of the lateral hemispheres, including the lateral ventricles (see Fig 3).

SECTION

1, 2-SAGI77”

MIDLINE

Two structures are brought into alignment in the midline plane: the highly echogenic vermis of the cerebellum and the corpus callosum (Fig 11). The cerebellar vermis is indented anteriorly by a small cleft in the fourth ventricle, the fastigium, which is the region where the foramina of Luschka and Magendie are located. One first sees the quadrigeminal plate extending anterosuperiorly from this region and then the inferior structures of the corpus callosum, starting at the splenium and curving gently anteriorly. Underneath this structure, the cavum septum pellucidi (anteriorly) or the vergae (posteriorly), or both, can be identified. immediately inferior, the third ventricle can be identified with the massa intermedia in two-thirds of normal infants. The hypothalamic region can occasionally be visualized quite clearly. All of these structures are usually better seen when the ventricular system is present. The third ventricle and the corpus callosum rep-

PARASAGITTAL

SECTIONS

3- 6

Slight lateral angulation of the transducer as well as a slight tailing away of the beam from the midline posteriorly permits visualization of the thalamus as an egg on its side closely hugged posteriorly by the choroid plexus (Fig 12). The choroid plexus extends superiorly to the level of the caudothalamic groove which can therefore be slightly echogenic. The caudate nucleus, anterior to the thalamus, can usually be visualized as it is slightly more echogenic than the thalamus. The glomus of the choroid plexus should be smooth and adjacent to the thalamus posteriorly within the occipital horn. Further angulation of the transducer laterally will visualize the Sylvian fissure with the pulsating middle cerebral artery. The middle cerebral artery branches can be seen in a triangular distribution over the cortex of the insula.

INDICATIONS

In the NICU it is important to separate clinical indications from screening indications.31-34 It has been clearly shown that ultrasound can identify and thus screen for ventricular dilatation and hemorrhage. Bleeding can occur intraparenchymally or intraventricularly, or may be limited to the germinal matrix. Most hemorrhages originate in the germinal matrix. Ultrasound provides the best means of following these abnormalities over time. It is, however, less useful in providing evi-

FIG 10. A, location

of section

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C, outstanding

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FIG 11. A, location of midline sagittal section; B, sonographic image; C, corresponding losum and vermis of cerebellum in one plane; c = cavum septum pellucldum

dence of increased intracranial pressure, parenchymal edema, sepsis or meningitis, or subdural or subarachnoid blood or CSF collections. Ultrasound can identify space-occupying lesions such as tumors, but it cannot be the final imaging modality before therapy is instituted. Ultrasonography is being used increasingly in interventional procedures of the neurocranium such as in the placement of ventriculoperitoneal shunts. Sonography plays a major role in screening of patients undergoing extracorporeal membrane oxbeygenation.35 The possibility of brain infarction cause of embolic events secondary to ligation of 102

anatomic section; D, and vergae, frequently

outstanding

landmarks:

corpus Cal.

identifiable.

the ipsilateral carotid artery and jugular vein is obvious as is the possibility of hemorrhage during anticoagulation therapy. Both edema and hemorrhage are twice as likely to occur in the presence of preexisting complications such as previous hemorrhage or leukomalacia.3” Most infants considered for extracorporeal membrane oxygenation will therefore have a cranial ultrasound examination as part of the work-up because intracranial hemorrhage larger than a germinal matrix hemorrhage definitely contraindicates the procedure. Some centers will not institute extracorporeal membrane oxygenation if hemorrhage of any kind Curr

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FIG 12. A, location

of the parasagittal

sections:

B, sonographic

example;

C, outstanding

has occurred. It is, however, generally agreed that subdural or subarachnoid hemorrhage is not a contraindication to the procedure.35 The reason for this caution is that, if hemorrhage develops after extracorporeal membrane oxygenation has begun, it may be necessary to stop the procedure and the infant may die. More work being done on the flow characteristics of patients receiving extracorporeal membrane oxygenation will probably enhance the role of ultrasound screening in these infants .24,25,36,37 The incidence of hemorrhage varies between premature and term babies. Several studies have described a 5% to 50% incidence of hemorrhage in prematures, whereas term babies do not exhibit evidence of hemorrhage nearly so often.33’ 34 If all prematures had a screening cranial ultrasound, between 10% to 30% would manifest an abnormality. Such abnormalities are, however, seldom intraparenchymal; they are more frequently germinal matrix or ventricular hemorrhage, and/or ventricular dilatation.33 Clinical indications for ultrasound imaging in the NICU primarily oonsist of a drop in the hematocrit or a neurologic change. In the term infant, abnormalities, dysmorphism, (i.e., craniofacial meningomyeloceles, trisomy 18, or Down’s syndrome), seizures, and low APGAR scores (less than 7) are associated with positive findings in a significant number of patients. On the other hand, increased head circumference, a bulging fontanelle, or abnormal neurological examinations seldom result in significant, sonographically detectable abnormalities.34 Other modalities are available for evaluating the neonatal cranium. Computed tomography should, however, be reserved, for infants whose gestational Curr

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landmark:

thalamus;

e = egg-on-side.

and actual ages total more than 40 weeks.38 The sensitivity and specificity of CT findings are then more reliable, which in certain patients, may make CT more useful than sonography especially in follow-up or trauma studies. The potential of Magnetic Resonance Imaging (MRI) is unclear as yet since the technologv is obviously not portable and many contraindications to high magnetic fields exist in patients who are cared for in an intensive care nursery. It is difficult to provide necessary support and monitoring within the magnet. However, MRI is likely to become more important in view of its unique capability to image normal and abnormal myelination, its superb contrast resolution and its multiplanar imaging capability.3sJ 4o Ionizing radiation is a risk only in CT examinations, but the benefits of CT in the follow-up of surgical procedures and in assessing brain edema/ atrophy outweigh the inherent risks and therefore make it preferable to ultrasound in these clinical situations. MRI may supplant CT in these settings in the near future. There is significant controversy regarding the proper timing of cranial ultrasonography in the premature neonate.33 The high incidence, prognostic implications, and potential complications of germinal matrix and intraventricular hemorrhage justify an initial ultrasound in patients younger than 32 weeks’ gestation or less than 1500 g birth weight. Unless major neurological changes occur or there is a clinical change, such as a significant drop in the hematocrit, this initial scan can be performed within the first week of life. One-third of premature neonates with a normal study on day one may develop subependymal intracranial hemorrhage before the end of the first week of life.41 However, an initial normal study does not obviate 103

C, anatomical

correlation

of a Grade

1 germinal

matrix

hemorrhage.

further studies if there is a change in the clinical condition. Such changes may include blood pressure changes or the development of hypocoagulation states, necrotizing enterocolitis or pneumothoraces. If the initial study is positive for intraventricular or periventricular hemorrhage, one week follow-up to assess the extent and sequelae of the hemorrhage is recommended.

CLASSIFICATION OF INTFUCFtANIAL HEMORRHAGES Several investigators have developed grading systems to facilitate an orderly approach and predict outcomes in these premature infants with hemorrhage on screening cranial sonograms.41-43 These grading systems were based either on ultrasound or CT data.” 43 The early systems were based on CT findings, which are less specific, but probably more sensitive, than sonographic evaluation of the neonatal brain in the first 24-48 hours. Some of the ultrasound-based grading systems were obtained with older equipment whose resolution was poorer. The grading scheme presented here has been arrived at by combining imaging6” and clinical criteria. Any grading system is an attempt to use imaging information to arrive at a clinical prognosis. As this process is imprecise, no rigid conclusions can be stated. However, the basic four gradations are easily remembered: Grade 1 is an isolated germinal matrix hemorrhage (Fig 13). Grades 2 and 3 are small or large intraventricular hemorrhages (Figs 14 and 15) and Grade 4 is parenchymal extension of an intraventricular bleed (Fig 16). Grade l-Hemorrhage is contained in the subependymal region of the germinal matrix just anterior to the caudothalamic groove.

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FIG 14. A, clot (c) extending from choroid plexus in a minimally dilated occipital horn; B, germinal matrix hemorrhage and irregularity of the choroid plexus suggesting hemorrhage within it with associated ventricular dilatation.

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.-.---,

*-------D

----

nclude spastic@, rigidity, or mental retardation41 The quality of life predictable for these infants is a difficult determination; however, as a general rule, the larger the hemorrhage, the poorer the prognosis seems to

FIG 15.

Grade 2- Intraventricular hemorrhage without dilatation of the ventricle. This can also include hemorrhage within the choroid plexus as well. Grade 3- Intraventricular hemorrhage with dilatation of the ventricle. Grade 4- Intraventricular hemorrhage with parenchymal extension. With small lesions such as Grade 1 and 2, surviva1 is the rule. Moderate hemorrhage carries a low mortality rate (approximately 10Y01 and a low

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A, coronal view, se&Ion 1, reveals parenchymal hemorrhage on the right with midline shift to the left (small arrows); B, saglttal view reveals parenchymal extension of a germinal matrix hemorrhage Into the ventricles.

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PATHOGENESIS INTHACHANL4L

OF NEONATAL HEMOHHHAGE

Most intracranial hemorrhages in the preterm neonate occur in the area just anterior to the caudothalamic groove, the subependymal germinal matrix43 (Figs 17 and 18). The ependyma is a single layer of cells that lines the ventricles. The germinal matrix contains abundant delicate vasculature and is highly active metabolically. It consists of proliferating neuroectodermal cells that appear along the lateral ventricular margin during embryonic development. The vasculature of the germinal matrix is extremely friable between 24 and 32 weeks of gestation. Later, mature neuroectodermal cells migrate to the cerebral cortex, and the germinal matrix ceases to exist. The cells and vessels of the germinal matrix have very little supporting stroma and are vulnerable to a variety of hypoxemic or ischemic stresses. Conditions in which the cerebral blood flow is increased, such as apnea, intracardiac shunts, suctioning, and rapid volume expansion have been implicated as causes, whereas disseminated intravascular coagulation, hypernatremia, and hypercarbia as well as disturbances of vascular autoregulation are established causes of hemorrhage in the germinal matrix. On a cellular level, anatomic peculiarities of the deep venous drainage are also etiologically important, as is an inherent anticoagulant substance found in the germinal matrix.41 Many authors have stated that the overwhelming majority of intraventricular hemorrhages in premature infants result from transependymal rupture of a germinal matrix vessel. The choroid

Medullary

Foramen

Veins

of

Monro

-

1

FIG 17. Illustration 106

of venous

pattern

In germinal

matrix

Medullary

For ‘amen

Veins

of

Monro

Germinal

-LA

-

Matrix

FIG 18. Illustration

of motor

pathway

through

germinal

matrix

plexus has, however, also been implicated as a site of bleeding that extends into the ventricles, and the differentiation of bleeding at this site from germinal matrix hemorrhage is difficult. In addition, choroid plexus hemorrhage may itself be difficult to evaluate, The choroid plexus is largest in the region of the trigone (the glomus), and it should be entirely smooth. Anteriorly, the choroid plexus extends through the foramen of Monro and lies along the roof of the third ventricle. Any disturbance of the smooth contour of the choroid plexus denotes pathology, usually hemorrhage. Whether this is surface hemorrhage or intrachoroid hemorrhage is as yet controversial. In premature infants a “lumpy/bumpy” appearance of the choroid plexus suggests hemorrhage although the usefulness of this sign decreases when other abnormalities are present and when the baby is at term age. The normal choroid plexus pulsates; clot does not. With Doppler, this is a useful distinction. Posthemorrhagic dilatation of the ventricles is presumed to result directly from the presence of free blood in the CSF.44,45 It is thought to be more pronounced with higher grades of hemorrhage. The cause of ventricular dilatation may probably be sought in the damage to the various structures through which CSF flows. These include the foramen of Monro, the aqueduct of Sylvius, and the foramina of Luschka and Magendie. The areas where CSF is normally resorbed, the arachnoid granulations, can also be affected by this hemorrhage and, by absorbing less CSF, which can contribute to ventricular dilatation. Curr

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VENTRICULAR

DILATATION

In summary, the larger the hemorrhage, the greater are the frequency and severity of ventricular dilatation. This ventricular dilatation may be self-limited and eventually return to normal or stabilize. In the most severe Grade 3 and in most Grade 4 hemorrhages, shunting of the CSF is required. Persistent ventriculomegaly may frequently be observed over a period of months to years, although the consensus is that ventriculomegaly is self-limited in the majority of cases.44 In those ba-

bies in whom progressive ventricular enlargement occurs, the decision to place a shunt is a neurosurgical one and is normally taken after serial lumbar punctures have become ineffective in decreasing the ventricular dilatation. Sonographic determination of ventricular size can be quantitated by measuring lateral ventricular size on coronal scans obtained through the body of the lateral ventricles in a plane that includes the third ventricle. Ventricular depths and widths have been defined by Sauerbrei et al. and Fiske et al. as being useful measurements in following the development of ventricular dilatation.ti4.4” Anatomical measurements plotted against independent variables such as postconception age, weight, or head circumference resulted in the socalled “one-third rule,“47 which states that the ventricles on coronal scans should not occupy more than 33% of the entire hemisphere. This study, by Poland et al., did not include abnormal patients so that its value in differentiating normal from abnormal is untested. Thus, all of these measurements are most useful only for establishing a baseline for comparison with follow-up studies. Qualitative assessment of ventricular size is therefore more useful in practice than are quantitative measurements.47 Two useful signs include progressive rounding of the superolateral angles of the frontal horns and dilatation of the occipital horns (Fig 19). The size of the occipital horns is, however, highly variable, and one should not rely too much on these structures.48 For example, in the follow-up of neonates with hemorrhage and/or atrophy or ventricular dilatation, ventriculomegaly may coexist with atrophy, thus rendering quantitative assessment less useful. INTHAPAHENCHYMAL

FIG 19. A, coronal Image revealing asymmetrlc iar dilatation; B, sagittal view showing Curr

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ventrlcu-

HEMORRHAGE

Hemorrhage into the brain parenchyma can occur as a sequela of germinal matrix hemorrhage, birth trauma, Rh incompatibility, or other vascular insults (Fig 20). Although these latter causes are not the focus of this discussion, the result of all previously mentioned intracerebral hemorrhages is the same: porencephaly, replacement of damaged brain tissue by CSF. The size of porencephaly has been proven to be directly correlated to the size of the original parenchymal hemorrhage.43 The hematoma becomes hypoechoic within a few days to weeks. With further maturation echogenic borders appear, and the anechoic center becomes the focus of clot retraction. After the clot dissipates, the defect left behind is occupied by anechoic CSF. This process may take weeks to months. 107

FIG 20. A, coronal in nage of parenchymal hemorrhage to infarction: porencephaly; c, porencephalic

due to infarction (arrow); B, axial image region in the area of previous hemorrhage,

Hemorrhage other than intraventricular hemorrhage is not related to the germinal matrix. Intracranial hemorrhages in term or older infants are rare and are usually due to perinatal trauma or coagulopathy. Not only is the imaging of acute hemorrhage at least as easily done with CT as it is with ultrasound, the subarachnoid, subdural and epidural regions are much better evaluated by CT. Chronic subarachnoid or subdural hemorrhages may be missed on CT but will also not be easily identifiable on ultrasound. These are regions where MRI holds significant promise.

NONHEMORRHAGIC PERIVENTRICULM

INSULTS LEUKOh4ALACIA

Periventricular infarction of cerebral manifested by increased echogenicity 108

tissues is projecting

of the sequelae CT correlation.

of parenchymal

hemorrhage

due

off the lateral ventricles which, on sequential scans, may be seen to transform into cystic areas. This transformation is known as periventricular leukomalacia and occurs in 5% to 10% of premature infants.4s-52 This presumed hypoxemic brain damage causes white matter necrosis.“3, 54 It was first described more than a century ago by Virchow and was thought, in the ensuing years, to be related to perinatal circulatory insufficiency. The commonly involved areas adjacent to the trigone of the lateral ventricles and at the level of the foramen of Monro are similar in that they are watershed areas of the arterial blood flow (Fig 21). Not only necrosis, but also hemorrhage into the infarcted area may increase the damage. Since the neurodevelopmental prognosis for periventricular leukomalacia is poor, it is important to detect these changes early to psychologically prepare parents and personnel.““, 56 Cut-r

Probl

Diagn

Radiol,

May-

June

1991

FIG 21. A, coronal the lower

in Pel ,iventricular of c ystlc (:hanges resolution of CT compared with ultrasound.

leukomalacia;

6, sagittal

In the acute phase, broad zones of increased periventricular echogenicity are noted.57 These zones can be symmetrical but do not need to be homogeneous. It may be difficult to distinguish this appearance from the periventricular echogenie halo created by the normally dense venous plexus and radiating optic fibers surrounding the lateral ventricles. After the initial insult, liquefactions occurs, and small cysts that may not be visible on CT start to appear on ultrasound5” 5s (Fig Zl,C). Long-term changes depend on whether or not hemorrhage has occurred.6o The periventricular leukomalacic changes that appear two to three weeks after the appearance of the echodense areas produce a “swiss cheese” appearance in these watershed areas but may also involve the entire brain parenchyma (see Fig 21, A and B). As already noted, ultrasound is not very sensitive in detecting early periventricular white matter lesions and MRI might become the imaging Curr

Probl

Diagn

Radial,

May-

June

1991

view

of the changes;

C, CT scan at the same

time

illl Jstrating

modality of choice were it not for the inherent difficulty of obtaining the examination.fil It is important to differentiate porencephaly from necrosis because, according to some authors, it is important to define porencephaly as either secondary to intraparenchymal hemorrhage or to infarction that has cavitated.“’ Porencephaly differs from the cysts of periventricular leukomalacia in several respects: Porencephaly seldom disappears over time; it most often represents an extension of the ipsilateral ventricle or subarachnoid space, whereas periventricular leukomalacia does not. A further distinction is that porencephaly is almost always asymmetric; in periventricular leukomalacia a high degree of symmetry is preserved.“’ Major long-term clinical outcomes of periventricular leukomalacia include spastic diplegia and intellectual deficits. Spastic diplegia affects the lower extremities more than the upper extremities. Porencephalic changes 109

cause spastic hemiparesis and intellectual deficits as well.“” We have attempted to correlate the outcomes of various types of cerebral injury with their sonographic appearances. Whether cranial ultrasound can play a role in predicting or ameliorating these lesions remains to be seen. CEREBRAL INFARCTION In a post-term infant, isolated cerebral infarction is unusual.6” Although CT is the diagnostic modality of choice here and is necessary for adequate initial evaluation, ultrasound has been valuable in following the changes of cerebral infarction. Diffuse cerebral edema is difficult to evaluate on ultrasound, and definite neurologic findings are frequently not present (Fig 231. Embolic or ischemic

FIG 22. A, coronal

view the anterofrontal 110

reveals region

increased echogerxcity (arrow); C, CT correlation

right laterally of the right

stroke, although unusual, can occur in the newborn and can occasionally be found in patients being screened for extracorporeal membrane oxygenation or who have neurologic symptoms. The most common symptoms are hypotonia, lethargv, and/or seizures, Findings of cerebral edema include loss of normal gyral and sulcal anatomy and absence of vascular pulsations. Embolic strokes, especially in the setting of extracorporeal membrane oxygenation and umbilical catheters, are recognizable by ultrasound or CT (Fig 221. These lesions are located peripherally and may be missed on the routine views.63 INFL,4Mh4ATION Almost one-third of patients with meningitis have intracranial involvement (Fig 24). Imaging of

(arrow); B, parasagittal frontal lschemic event.

view

reveals

Curr

Increased

Probl

echogenicity,

Diagn

Radiol,

III defined

May-

June

in

1991

FIG 23. Loss of cortical markings and loss of definition of the intracranial structures suggesting intracranial edema in this 44.week infant.

the brain parenchyma is useful for identifying and following the sequelae of intracranial infection.“4 The ultrasonographic findings of meningitis include echogenic sulci, seen in about 40% of patients, and extra-axial fluid collections, frequently observed in bacterial meningitis.64 If ultrasound displays the crowns of cortical gyri along the convexity, an extra-axial fluid collection has displaced brain and the ultrasound evaluation is diagnostic of the fluid collection. These collections displace the gyri along the convexity and interhemispheric fissure. Similar fluid can also be seen in the interhemispheric fissure. Ventricular dilatation may or may not be associated with meningitis. More subtle findings include abnormal parenchymal echogenicity. This finding is nonspecific and is highly subjective. The lesions may be patchy, localized or diffuse, unilateral or bilateral, and are quite small. Abscess formation and cystic degeneration are much easier to localize. Ventriculitis is the most easily identifiable ultrasonographic finding.65 It occurs in 65% to 90% of cases of neonatal bacterial meningitis and is important as it is associated with an increase in mortality and neurologic sequelae. The normally thin and smooth ventricular wall becomes thickened, hyperechoic, and irregular, probably because of the presence of debris and exudate. By the second or third week, debris may be seen within the CSF, and strand-like, fibrinous bands may appear. Disappearance of this material during recovery can be effectively monitored by ultrasound; however, meningeal involvement is difficult to identify. Its sequelae, brain infarction and/or subdural hemorrhage or abscess formation, are better imaged by CT or MRI. Curr

Probl

Oiagn

Radial,

May-

June

1991

Intrauterine infections have recently been shown to cause frond-like calcifications in the basal ganglia. These have proven to be thrombosed vessels or perivascular mineral depositions that can easily be identifiede6 (Fig 251. This appearance has been seen with some of the TORCH infections (rubella, toxoplasmosis, herpes) and AIDS, and it also seems to be associated with congenital cardiac abnormalities or trisomy 21. The classical gross calcifications known to be associated with TORCH and noted on plain film as well as on CT are not as clearly seen with MRI. Another of the TORCH infections, Herpes Simplex Virus II, causes a particular pattern of brain abnormality. Brain involvement is diffuse in neonatal herpes encephalitis. Within the first 3 to 4 weeks of life, changes of edema may be observed. During the next two weeks the edema progresses, resulting in ventricular compression. By 5 to 6 weeks the ventricles begin to enlarge with changes of encephalomalacia. The initial formation of cystic encephalomalacia may be more apparent on ultrasound than on CT”““’ (Fig 26). CYSTIC LESIONS DAhVlY-WALKER

CYST

The Dandy-Walker cyst is a commonly seen abnormality in infants and is characterized by enlargement of the fourth ventricle secondary to absence of the inferior cerebellar vermis and atresia of the foramina of Luschka and Magendie. The vermis abnormalities can be minute or may involve the entire vermis as well as the cerebellar hemispheres. The CSF flow is a matter of controversy. 111

FIG 24. Two-week-old wrth signs and symptoms B, coronal sectlon 1 week later reveals nold space; D, CT correlation. (Courtesy 112

of menlngitls. A, coronal sectlon wtdened Interhemispheric fissure Kathleen McCarten, M.D.)

reveals (arrows);

normal InterhemIspheric C, linear array close-up

Curt- Probl

fissure on this screening study; of debris (arrow) In subarach-

Diagn

Hadiol,

May-

June

1991

There are those who maintain that there is a specific cyst, which is encapsulated.“’ Therefore shunting of the cyst would be curative for the ventricular dilatation caused by this malformation. Other possible etiologies for the Dandy-Walker appearance in the posterior fossa suggest either that the agenesis of the cerebellar vermis causes enlargement of the fourth ventricle or, conversely, that an obstruction distal to the fourth ventricle causes vermian dysgenesis. There are no specific clinical symptoms associated with this malformation except those secondary to the ventricular dilatation, if present. Ultrasound shows a large cystic area in the posterior fossa corresponding to the dilated fourth ventricle6’ (Fig 27, A and B). The tentorium is flattened, and there are variable degrees of cerebral hemisphere dysplasia. The occipital horns and the third ventricle may be dilated depending on how much obstruction of the CSF flow has occurred. The Dandy-Walker cyst is occasionally associated with agenesis of the corpus callosum and interhemispheric arachnoid cysts (Fig 27,C). ARACHNOID

FIG 25. A, coronal view demonstrates increased echogenic fronds basal ganglia: 6, sagittal view reveals increased echogenic tures in the thalamus in a patient with AIDS.

in both struc-

CYSTS

Most arachnoid cysts are usually found in the middle cranial fossa, adjacent to the temporal lobes. These are subarachnoid lesions that may displace the cerebellum and fourth ventricle. This CSF collection may be congenital, due to abnormal leptomeningeal formation, or acquired as a result of entrapment of arachnoid CSF by arachnoid adhesions. The symptoms result from the ventricular dilatation (Fig 28).

PORENCEPHALIC

CYSTS

As mentioned above, these cavities containing CSF are almost always associated with ventricular dilatation. They are not lined by true ependyma and may be congenital (possibly undetected intrauterine grade 4 hemorrhages). They are most often acquired secondary to postnatal destruction of cerebral tissue by hemorrhage, infection, or trauma.

VEIN FIG 26. Coronal view in a patient with herpes simplex type II reveals encephalomalacic changes bilaterally. (From Cleveland RH, Herman TE, Oot RF, et al: Am J Perinatology; 4:215-219. Used by permission) Curr

Probl

Diagn

Radio&

May-

June

1991

OF GALEN

ANEURYSM

This is a rare arteriovenous malformation that frequently presents with high output congestive heart failure. Pulsations can be seen sonographitally, and with Doppler evaluation the typical arterial curves are seen in the arterial component. A 113

FIG 27. A, coronal B, sagittal

view view

reveals a cystic lesion in the posterior fossa confirming the cystic nature of the posterior

with rudimentary cerebral peduncles fossa; C, CT image confirms classic

bruit can frequently be heard as we11.6o The location of the aneurysm is classic with a tubular structure seen in the region of the quadrigeminal plate cistern. Its course lies in the direction of the straight sinus, in the midline.

HOLOPROSENCEPHALY

When the prosencephalon fails to divide properly between the fifth and sixth weeks of embryogenesis the paired appearance of the ventricles and parenchyma fails to develop. This failure results in a spectrum of lobar, alobar or semilobar holoprosencephaly, a direct reflection of the severity of the embryologic insult and the stage at which it occurred. 7o There is no third ventricle or septum pellucidurn, and this 114

immediately inferior to the tentorium findings of Dandy-Walker syndrome.

(f);

appearance is frequently diagnostic. The diagnostic findings include a midline thalamic mass and the absence of the falx cerebri, which distinguish this entity from hydranencephaly. The fusion is frontal in the milder cases. Holoprosencephaly is characterized by a midline thalamic mass, absence of the falx cerebri and, depending on the degree of nondiverticularization of the fetal brain, a horseshoe-shaped single ventricular cavity (Fig 291. Mortality is high. Clinical symptoms are related to the remaining functional brain tissue. Holoprosencephaly may be associated with other anomalies including maternal diabetes, trisomy 13-15 or trisomy 18, intrauterine rubella, and other endocrine abnormalities. There are often associated midline facial anomalies ranging from cyclopia to cebocephaly. Curr

Probl

Diagn

Radio&

May-

June

1991

FIG 28. A, c oronal ultra sound section reveals a cystic lesion in the midbrain, cyst in another patient, coronal section; D, transfontanel metrizamids

in the same c)n the right; B, MR correlation ? CT study illustrates noncommunication

patient; C, midline arachr ioid of the cyst with the CSF f low.

FIG 29. Coronal cerebri.

Curr

Probl

Oiagn

Radio&

May-

June

1991

section

of holoprosencephaly

revealing

absence

of the falx

115

SOLID

LESIONS

ARNOLD-CHL4RI

MALFOZUbfATION

This malformation includes elongation of the pons and fourth ventricle and downward displacement of the medulla and fourth ventricle into the cervical spinal canal with a relatively small posterior fossa. The Arnold-Chiari malformation is frequently associated with some form of spinal dysraphism, usually a meningomyelocele. Type 1 represents downward displacement of the cerebellar tonsils and inferior cerebellum; Type 2 represents downward displacement of the cerebellar medulla and fourth ventricle into the spinal cord and is always associated with a meningomyelocele; Type 3 is characterized by displacement of most of the cerebellum into a high cervical/occipital meningocele. The ventricular dilatation may be asymmetric, and the lateral ventricles are characteristically pointed inferiorly with a medial concavity of the frontal horns. The frontal horns frequently are slitlike, whereas the atria and occipital horns are dilated to varying degrees. There is frequently an enlarged massa intermedia and a prominent inferior commissure. A wide variety of clinical symptoms are associated with this abnormality; their manifestation depends in large measure on how much herniation of the brain stem and cerebellum has occurred. AGENESZS

OF THE

CORPUS

CALLOSUM

The corpus callosum is the principal tract connecting the right and left cerebral hemispheres and may be partially or completely absent. It normally forms the roof of the third ventricle. The frontal horns can be thought of as being held together by t.his midline connecting structure.

Therefore the frontal horns will be widely separated in the absence of the corpus callosum, and the third ventricle will herniate superiorly into the space created (Fig 301. The interhemispheric fissure is also widened. The vessels and gvral markings are seen to be arranged radially. Probst bundles are bundles of white matter in the medial walls of the ventricles. They cause concave medial borders of the lateral ventricles.728 73 Many causes such as genetic, metabolic and mechanical factors involving the commissural plate early in development have been implicated to explain the absence of the corpus callosum in its varying stages. Such absence may exist as an isolated lesion or as part of other anomalies such as Dandy-Walker cyst, Arnold-Chiari malformations, the spectrum of holoprosencephaly, or other entities. No symptoms are associated with absence of the corpus callosum; if symptoms are present they are usually explained entirely by the associated abnormalities, previously discussed. There may, therefore be no abnormal neurological or developmental findings.74 MZGZVITZONAL

DISORDERS

OF THE

BRAIN

Disturbances of neuronal migration produce abnormal development of the parenchymal cortex resulting in lissencephaly, heterotopias, and thick or thin gyri. Clefts (schizencephaly) result from localized migration failure. These disorders are frequently bilateral and may be symmetrical75 (Fig 31). CONCLUSION

Ultrasonography ety of intracranial

is used to evaluate a wide variabnormalities in the premature

FIG 30. A, midline sagittal view reveals absence of the gyral markings (arrow); B, absence tal structures (arrow); C, MR correlation 116

of the corpus callosum in the plane the cerebellar of vermis (v). Note the fan-shaped orientation of the corpus callosum: Coronal view reveals radiating gyri and absence of the paired horizonin absence of the corpus callosum. Curr

Probl

Diagn

Radio/,

May-

June

1991

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