Review

Richard A. Bowerman1

Steven M. Donn2

Terry M. Silver1

Mark H. Jaffe1.3

This article appears in the September/Octo­ber 1984 issue of AJNR and the November 1984 issue of AJR.

Received September 26, 1983; accepted after revision April 9, 1984.

1 Department of Radiology, Box 013, Division of Ultrasound, University of Michigan Medical Center, Ann Arbor, MI 48109. Address reprint requests to R. A. Bowerman.

2 Department of Pediatrics, Section of Newborn Services, University of Michigan Medical Center, Ann Arbor, M148109.

3 Present address: Department of Radiology, Georgetown University Hospital , Washington , DC 20007.

AJNR 5:527-538. September/October 1984 0195-6108/84/0505-0527 © American Roentgen Ray Society

527

Natural History of Neonatal Periventricular / Intraventricular Hemorrhage and Its Complications: Sonographic Observations

Cranial sonography is an established procedure for the detection of neonatal intra­cranial hemorrhage. A 3 year experience in imaging such infants is reviewed. Repre­sentative examples are presented to comprehensively illustrate the spectrum of sono­graphic appearances of intracranial hemorrhage and its complications from the initial hemorrhage to resolution. Diagnostic problems in the initial staging of the grade of hemorrhage and in evaluating subsequent ventricular changes are addressed.

The incidence of intracranial hemorrhage in premature infants of less than 35 weeks gestational age or 1500 g birth weight is 31 %-55% by computed tomog­raphy (CT) [1-4] and sonography [5- 10]. and is reportedly as high as 70% if assisted respiration is used [11]. Posthemorrhagic hydrocephalus. often clinically silent [12-14]. is a complication that. if diagnosed early. may be treated conserv­atively [15]. but. if diagnosed late. may have serious long-term consequences.

Previous reports on neonatal cranial sonography have described examination techniques [16-21] and clarified the sonographic appearance of normal intracranial anatomy [16-18.22-24]. hydrocephalus [25-31] . isolated examples of intracranial hemorrhage [19.32- 34]. and miscellaneous other intracranial abnormalities [35-38]. Other articles have outlined a more general overview of the utility of cranial sonography [18. 39-53].

This report provides an organized. comprehensive. and longitudinal sonographic analysis of the evolution and natural history of intracranial hemorrhage. stressing the initial sonographic patterns of germinal matrix. intraventricular. and intracerebral hemorrhage and their changing sonographic appearance over time. The sono­graphic evolution of ventricular changes. including hydrocephalus and poren­cephaly. will be discussed and illustrated with emphasis on their relation to the location and severity of the initial intracranial hemorrhage.

Materials and Methods

A total of 1743 neonatal cranial sonographic examinations were performed between May 1979 and July 1982, predominantly in infants admitted to the Holden Neonatal Intensive Care Unit of the University of Michigan Medical Center. The indications for routine sonographic screening were an infant of birth weight less than 1500 g or gestational age less than 35 weeks. Other infants suspected of having intracranial hemorrhage by clinical or laboratory parameters were also examined.

Most studies were performed with an ATL mechanical real-time sector scanner (Advanced Technology Labs .• Bellevue. WA). Technicare MCU (Technicare Corp .• Cleveland) and ATL Neuro SectOR real-time sector scanners were used on some of the more recent cases. The examinations were performed with a 5 MHz or 7.5 MHz (rarely) transducer through the anterior fontanelle [54] . Sequential sonograms were obtained in the coronal and sagittal planes by angling the transducer to maximally visualize the entire ventricular system and as far peripherally into the brain substance as possible.

528 BOWERMAN ET AL. AJNR:5, Sept/Oct 1984

1 2

Fig. 1.-Coronal sonogram shows uniformly echogenic left grade 1 hemor­rhage (arrow) at inferolateral aspect of left lateral ventricle. Lateral ventricular bodies (arrowheads).

Fig. 2.-Left parasagittal sonogram shows echogenic grade 1 hemorrhage at thalamocaudate notch superior to thalamus (T) and posterior to head of

A B

Results

The types of intracranial hemorrhage most amenable to sonographic diagnosis in the premature infant are peri vent ric­ular or intraventricular [53] . While several classification sys­tems for intracranial hemorrhage have been proposed [2, 55-61], the most widely accepted is that of Papile et al. [1]: grade 1-subependymal hemorrhage (germinal matrix); grade 2-intraventricular hemorrhage without ventricular dilatation; grade 3-intraventricular hemorrhage with ventricular dilata­tion; and grade 4-intraventricular hemorrhage with paren­chymal hemorrhage.

Grade 1 Hemorrhage

Initially, a grade 1 (subependymal or germinal matrix) hem­orrhage appears as a uniformly echogenic mass, typically at

3

caudate nucleus (C). P = choroid plexus in trigone of lateral ventricle. Fig. 3.-Coronal sonogram demonstrates right grade 1 hemorrhage (arrow­

head) compressing adjacent lateral ventricle. Normal left lateral ventricle (ar­row) .

Fig. 4.-Coronal sonograms in neonate. A, Right grade 1 hemorrhage (arrow). e, At 3 months of age. Residual punctate parenchymal echo (arrow­head) from otherwise resolved grade 1 hemor­rhage. Ventricles (V) are normal in size.

the level of the head or body of the caudate nucleus [40, 55, 62, 63]. On coronal sonograms, they are inferolateral to the lateral ventricle, at a level usually just posterior to the foramen of Monro (fig. 1). On sagittal images, smaller hemorrhages are generally observed in the "thalamocaudate notch," an anatomic area superior to the body of the thalamus and posterior to the head of the caudate nucleus (fig. 2). Grade 1 hemorrhages may be of variable size, and larger hemorrhages may extend anteriorly to a variable extent and even encom­pass the entire head of the caudate nucleus [64]. Subepen­dymal hemorrhages may be uni- or bilateral, and may be isolated or found in combination with more extensive hemor­rhage. Associated focal ventricular compression at the infer­olateral aspect of the ventricle is seen with larger hemor­rhages (fig. 3).

Several evolutionary pathways are available for an isolated grade 1 hemorrhage. The initial lesion may regress, decreas-

AJNR:5, Sept/Oct 1984 SONOGRAPHY OF NEONATAL INTRAVENTRICULAR HEMORRHAGE 529

Fig. 5.-Coronal (A) and left parasagittal (B) sonograms demonstrate focal cystic area of poren­cephaly (subependymal cyst) (arrows) in location of prior grade 1 hemorrhage. T = thalamus; C = cavum septi pellucidi; V = ventricle; A = anterior.

Fig. 6.-Coronal sonograms. A, At 2 days of age. Small right grade 1 hemorrhage (arrow) . Nor­mal-sized lateral ventricles. B, 4 days of age. Inter­val extension of extensive hemorrhage into dilated right lateral (large arrow) and third (small arrow) ventricles (grade 3 hemorrhage).

A

ing gradually in size and echogenicity until complete resorp­tion results in normal sonographic brain texture. Occasionally, a residual linear or punctate echo (fig. 4) is identified, and not infrequently, a focal area of porencephaly (subependymal cyst) of 3-5 mm results [47] (fig. 5).

Grade 1 hemorrhages may also enlarge mildly without change in grade, with subsequent regression or progression as described below. The most common form of extension is directly into the ventricular system, occurring in about 80% of subependymal hemorrhages [40, 55, 65, 66] (fig. 6). Sig­nificant enlargement of a grade 1 hemorrhage may result in isolated extension into the adjacent parenchyma. However, combinations of both intraventricular and intraparenchymal extension are the most common findings when intraparenchy­mal hemorrhage is present beyond the germinal matrix. With a grade 1 hemorrhage that does not extend into the ventric­ular system, the ventricles usually retain a normal size (fig. 4).

Grade 2 Hemorrhage

Blood within a nondistended ventricular system is classified as a grade 2 hemorrhage. The identification of increased

B

echoes that conform to part or all of the ventricular shape is necessary for this diagnosis. A small amount of blood may be difficult to identify within a nondistended ventricle, or to dif­ferentiate from a grade 1 hemorrhage, inasmuch as the former tends to represent direct extension of the latter [65]. Identifi­cation of clot within the occipital hom or of a blood-cerebro­spinal fluid (CSF) level in the dependent part of the ventricular system may be the only indication of a grade 2 hemorrhage [39, 53, 67] (fig. 7). Thus, sonograms obtained with the head in different dependent positions, if feasible, may be required to establish the correct grade. Sagittal sonograms are also more useful than coronal images in this differentiation. More extensive grade 2 hemorrhages are easier to identify (fig. 8). However, caution should be exercised to differentiate intra­ventricular hemorrhage from the normal choroid plexus [68, 69], which at times can appear quite prominent, especially in the trigone and occipital hom (fig. 9). The latter extends from the roof of the third ventricle through the foramen of Monro and along the floor of the body of the lateral ventricle into the trigone, where it enlarges before extending along the roof of the temporal horn. The choroid plexus in the lateral ventricles should be symmetric, with a smooth tapering configuration

530 BOWERMAN ET AL. AJNR:5, Sept/Oct 1984

7 8

9 10

anterior to the trigone and no extension anterior to the fora­men of Monro [68] (fig . 10).

Grade 2 hemorrhages may evolve to grade 3 lesions either by further hemorrhage distending the ventricular system or with the development of ventriculomegaly. A small amount of intraventricular hemorrhage without progression may cause focal or mildly diffuse, but rarely moderate, ventricular enlarge­ment. However, with such nonprogressive grade 2 hemor­rhage, the ventricular system will generally evolve to a normal or mildly dilated status. Rarely, more pronounced ventriculo­megaly may develop secondary to a grade 2 hemorrhage, yet with prolonged follow-up considerable resolution generally results (fig. 11). The organization and resorption of intraven­tricular clot will be described subsequently.

Grade 3 Hemorrhage

Initially a fresh grade 3 hemorrhage is identified by seeing homogeneously increased echoes within the ventricular sys-

Fig. 7.-Parasagit1al sonogram demonstrates large grade 1 hemorrhage (arrow). Local extension into ventricle cannot be determined with certainty. Definite echogenic clot is in occipital horn (arrow­heads) , however, confirming intraventricular blood. A = anterior.

Fig. 8.-Parasagittal sonogram demonstrates small amount of echogenic blood nearly filling non­distended lateral ventricle (arrows) , extending from thalamocaudate notch into temporal horn. Distinc­tion from choroid plexus (C) is difficult due to similar echo texture. P = posterior.

Fig. 9.-Parasagittal sonogram shows very prominent, echogenic choroid plexus filling occipital horn (arrow) . No intraventricular hemorrhage was present at autopsy shortly thereafter.

Fig. 10.-Parasagittal sonogram demonstrates minimal intraventricular hemorrhage adjacent to choroid plexus (P). Intraventricular echoes in frontal horn represent hemorrhage (arrows), as choroid plexus is not located there. C = head of caudate nucleus.

tem conforming to part or all of an enlarged ventricle (fig . 12). Because of its usual extension from a germinal matrix hem­orrhage [55, 65], intraventricular hemorrhage is most often identified within the body of the lateral ventricle extending from the "thalamocaudate notch" region posteriad to a varia­ble extent (fig. 13). This pattern of extension may not be seen in the term neonate, where intraventricular hemorrhage usu­ally arises from the choroid plexus [62, 70-73]. Choroid plexus hemorrhage in premature neonates may also be more prevalent than previously suspected [74] . With a severe intra­ventricular hemorrhage, the entire ventricle fills with blood and has a "castlike" appearance (fig. 14). The amount of hemorrhage present within the lateral ventricles is often asym­metric. With more extensive hemorrhage, an associated grade 1 hemorrhage may not be discernible.

While the initial ventriculomegaly present with a grade 3 hemorrhage is generally from distension by hemorrhage, in short course, obstructive changes will lead to increased CSF volume within the ventricles. This is frequently the stage at which these infants are initially scanned, with the identification

AJNR:5, Sept/Oct 1984 SONOGRAPHY OF NEONATAL INTRAVENTRICULAR HEMORRHAGE 531

Fig. 11 .-Coronal sonograms. A, Moderate hy­drocephalus 3 weeks after grade 2 hemorrhage comparable to that in figure 10. B, Nearly complete resolution 8 weeks later.

12

A

13 Fig. 12.-Parasagittal sonogram shows intraventricular hemorrhage within

trigone and occipital horn of dilated ventricle (V), surrounding choroid plexus (C) of same echogenicity. P = posterior.

Fig. 13.-Parasagittal sonogram demonstrates maturing intraventricular clot (arrow) , which has extended posteriorly from germinal matrix at thalamocau-

Fig. 15.-Parasagittal sonograms. A, At 3 days of age. Heterogeneous hemorrhage (arrowheads) of lesser echogenicity than choroid plexus distrib­uted throughout dilated lateral ventricle. CSF can be seen in trigone and frontal and temporal horns. B, At 3V2 weeks of age. Internal clot maturation with hypoechoic centrum surrounded by echogenic margin . Worsening hydrocephalus. P = posterior.

A

B

14 date notch. Discontinuity of echogenic clot margins at point of origin of intraventricular clo\' C = head of caudate nucleus, T = thalamus.

Fig. 14.-Parasagittal sonogram shows complete filling of distended lateral ventricle with echogenic hemorrhage. P = posterior.

B

532 BOWERMAN ET AL. AJNR:5, Sept/Oct 1984

A B

A

c D

of a nonuniform and less echogenic clot with variable degrees of surrounding CSF in dilated ventricles (fig. 15A).

A predictable sequence of sonographic changes occurs during complete resorption of intraventricular hemorrhage over the course of weeks to months.

Fig. 16.-Parasagittal sonograms. A, Severe hy­drocephalus with old organized intraventricular clots in temporal horn (arrow) . B, After reverse somersault maneuver. Relocation of intraventricular clot to body of lateral ventricle (arrows) .

Fig. 17.-Parasagittal sonograms. A, 5 weeks of age. Old organized clot of varied sonographic character within posterior parts of dilated lateral ventricle (V). A = anterior. B, 2 months of age. Partial interval resorption and some fragmentation of intraventricular clot, with reduced ventriculome­galy. C, 2V2 months of age. Considerable interval resorption with residual clot only in occipital horn (arrowhead). Persistent ventricular septation/bar (arrow) and further mild reduction in caliber of ven­tricular body/frontal horn. D, Follow-up at 7 months of age. Minimal clot adherent to choroid plexus in trigone (arrowhead) and a few fine persistent intra­ventricular septations (arrows) . Pronounced interval worsening of hydrocephalus at stage when most intraventricular clot has been resolved.

The initial hemorrhage is uniformly echogenic, similar in echo texture to the choroid plexus, but distinctive in distri­bution and size. After the stabilization in size of the intraven­tricular hemorrhage, the interior of the clot gradually loses its echo texture and becomes increasingly hypoechoic in con-

AJNR:5, Sept/Oct 1984 SONOGRAPHY OF NEONATAL INTRAVENTRICULAR HEMORRHAGE 533

Fig. 18.-A, Midcoronal sonogram at level of foramina of Monro demonstrates marked hydro­cephalus. Residual left intraventricular clot (arrow­head). T = temporal horns, 3 = third ventricle. B, Posteriorly angled coronal sonogram shows mark­edly dilated lateral, thirc (3), and fourth (4) ventricles. Residual left intraventricular clot (arrowhead). C, Left sagittal sonogram demonstrates marked hy­drocephalus involving entire left lateral ventricle. Old intraventricular clot adherent to echogenic choroid plexus (arrowheads ) and layered dependently in occipital hom (arrows). Note thinned cerebral cor­tex, particularly posteriorly. 0 , Sagittal sonogram shows marked enlargement of fourth and third ven­tricles. V = body of left lateral ventride, A = anterior.

A

c

trast to a densely echogenic clot margin [47, 67, 75] (fig. 15B). The echogenic margin is often noted to be discontin­uous at the point of origin from the germinal matrix (fig. 13). There is gradual clot retraction with the clot becoming more apparent because of enlarging CSF spaces, relative or actual. Fragmentation occurs with loose parts of clot free to move within the ventricular system (figs. 16 and 17). Resorption of clot continues until there is complete clearing of the ventricular system. Occasionally a residual septation or bar persists (figs. 17C and 170).

Subsequent to a grade 3 hemorrhage, significant so no­graphic changes are noted with respect to both the hemor­rhage and ventricles. With grade 3 hemorrhage, there devel­ops mild to moderate ventriculomegaly, which sometimes is progressive (fig. 18), often requiring periodic lumbar puncture drainage, and in some cases necessitating diversionary shunt placement. However, after the resorption of all intraventricular clot, often there is significant reduction of ventricular size, and in our experience the end result of grade 3 intraventricular hemorrhage appears to be ventriculomegaly of a mild to moderate degree, which may be asymmetric. A few patients demonstrated late progression of hydrocephalus after appar-

B

o

ent stabilization of ventricular size and nearly complete clot resorption (fig. 17).

Occasionally one may note resolved or markedly reduced ventriculomegaly in infants with pronounced initial hemor­rhage or previously significant ventriculomegaly. Ventricular dilatation involving the third and fourth ventricles is less pronounced than lateral ventricular distension, and is not a uniform finding in all cases [76].

Grade 4 Hemorrhage

Intraventricular hemorrhage that extends into the brain parenchyma is termed grade 4 (fig. 19). As with other intra­cranial hemorrhages, the initial appearance of such a bleed is uniformly echogenic. Blending with an intraventricular c0m­

ponent often causes focal obscuration of the lateral ventricle on the side of involvement (fig. 20). An associated grade 1 hemorrhage mayor may not be apparent. With larger hem­orrhages, mass effects may be present, including depre ion of the sylvian fissure or a shift of the midline structure to the opposite side (fig. 20). The frontoparietal distribution is most common in our experience,

534 BOWERMAN ET AL. AJNR :5, Sept/Oct 1984

A 8

A 8

A 8

Fig. 21 .-Midcoronal sonograms. A, 3 days of age. Recent hemorrhage within third (arrowhead) and lateral (small arrows) ventricles with extension intracerebrally on right (large arrows). B, 25 days of age. Typical maturational changes of intraventricular clot (curved arrow) within dilated ventricles. Evolving intra parenchymal clot has become centrally hypoechoic, and superiorly its

c

Fig. 19.-Coronal sonograms. A, 2 days of age. Intraventricular hemorrhage distending lateral (ar­rows) and third (arrowhead) ventricles. B, At 9 days of age. Interval extension of extensive hemorrhage intracerebrally on left (arrows). Right lateral ventricle (V) can be seen becoming dilated secondary to intraventricular hemorrhage.

Fig . 20.-A, Midcoronal sonogram demon­strates marked mass effect from extensive left intraventricular/intracerebral hemorrhage with shift of right lateral ventricle (arrowhead) and cavum septi pellucidi (straight arrow) to right. Obscuration of ipsilateral ventricle. Midline (curved arrow). B, Left parasagittal sonogram shows extent of pa­renchymal hemorrhage (H) and mild depression of sylvian fissure (arrows) . A = anterior.

echogenic margin can be seen retracting from adjacent normal brain, with intervening septations (straight arrows). C, 5 months of age. Resultant com­municating porencephaly (P) from prior intra parenchymal hemorrhage, with residual but reduced ventriculomegaly from previous intraventricular hemor­rhage.

AJNR:5, Sept/Oct 1984 SONOGRAPHY OF NEONATAL INTRAVENTRICULAR HEMORRHAGE 535

Fig. 22.-A, Midcoronal sonogram at 10 days of age. Left intraparenchymal hemorrhage (arrows) . C = cavum septi pellucidi. e, Midcoronal sonogram at 6 months of age. Resultant porencephaly (P) of size and configuration similar to that of initial hemorrhage. Dilated left lateral ventricle (V). C, Left parasagittal

The sequential sonographic changes of an intraparenchy­mal hemorrhage are similar to intraventricular hemorrhages (fig. 21). The initial uniformly echogenic hemorrhage loses central echogenicity while a peripheral echogenic ring per­sists. Small cystic areas appear where the clot is liquefying centrally . Gradual retraction of the clot from the surrounding normal brain tissue leaves intervening septations of organized clot. Eventually there is further retraction, fragmentation, and resorption of clot, with the ultimate development of a poren­cephalic cyst over the course of several weeks to months [47,77,78] .

We have generally observed communication of the subse­quently developing porencephalic cyst with the adjacent ven­tricle [79]. Such posthemorrhagiC porencephaly conforms well to the configuration of the initial intracerebral hemorrhage (fig. 21) and is often associated with focal dilatation of the adjacent communicating ventricle (fig. 22).

Discussion

Intracranial hemorrhage is a significant problem in the low­birth-weight premature infant, with resultant hydrocephalus a serious complication. Neonatal morbidity and mortality is roughly proportional to the degree of intracranial hemorrhage [1,2,4,55,56,60,80-82]. A correlation between the severity of the intracranial hemorrhage and the subsequent degree of ventriculomegaly was found in our series and has been re­ported by others [2,12,47, 55,60,77,81-85]. The dynamic nature of progression of intraventricular and peri ventricular hemorrhage with potentially severe ventriculomegaly must be stressed. However, a significant number of patients with apparently pronounced posthemorrhagic ventriculomegaly improve with conservative therapy [7,86]. Sequential studies are necessary to document particularly the regression and resolution of intraventricular hemorrhage, and the stabilization of any resultant ventriculomegaly. Sonography is an accurate

sonogram at 6 months of age. Dilated ventricular body and frontal horn (V) at level of intraparenchymal hemorrhage. Remaining lateral ventricle is of normal size. No intraventricular hemorrhage was diagnosed sonographically or clinically during hospital stay. P = posterior.

and simple procedure well suited to such evaluation of the premature neonate. Serial examination may be performed with ease in the ambient environment of the infant 's isolette due to the portable nature of real-time sonography.

Cranial CT examinations were initially performed in addition to cranial sonography in about the first 30 neonates who could be transported safely. When the diagnostic accuracy of sonography became apparent in our series, as well as in other series [16, 47, 50, 55, 67 , 69, 75, 87-93], this practice was discontinued except in a few of the more complex cases. The infant was thus spared the risk of travel, sedation, and radiation inherent in cranial CT. While the most clinically important types of neonatal intracranial hemorrhages are those diagnosable readily by sonography [55] , note should be made of the inability of sonography to accurately image subarachnoid hemorrhage [89, 91] . In addition, the autopsy incidence of intracerebellar hemorrhage is 21 %-25% in pre­term neonates of 28-34 weeks gestational age [94, 95] ; however, the reported sonographic detection of such hem­orrhage is scant [96, 97]. This may relate to the inherent echogenicity of the cerebellar vermis [76] .

As outlined in Results , potential pitfalls exist in the differ­entiation of a grade 1 from a focal grade 2 hemorrhage adjacent to the caudate nucleus, and in the identification of a small amount of intraventricular blood [40 , 47 , 62 , 89]. How­ever, follow-up examinations to evaluate for progressive hem­orrhage or developing ventriculomegaly are indicated in both cases and should differentiate between the grade of hemor­rhage on the basis of ventricular changes.

The histologic explanation for the evolving sonographic character of intraventricular and intracerebral hemorrhage has been forwarded by Enzmann et al. [98]. Based on experimen­tally induced intracerebral hemorrhage in a canine model , the echogenic periphery of organizing hemorrhage was found to be caused by the continued presence of intact red blood cells , as opposed to the breakdown of cells centrally , resulting in a

536 BOWERMAN ET AL. AJNR:5, Sept/Oct 1984

hypoechoic sonographic appearance. Similar conclusions have been presented by Sigel et al. [99].

We have noted not only asymmetric posthemorrhagic en­largement of the lateral ventricles, but also variable distension of the third and fourth ventricles. Posthemorrhagic hydro­cephalus may be from inflammatory ependymitis; from ob­struction of the foramen of Monro, aqueduct of Sylvius, or fourth ventricular outflow foramina; or secondary to basilar arachnoiditis [3, 85, 100]. Cisternography may playa role in defining the level, degree, and functional significance of these obstructions [101, 102].

In addition, we suggest the need to expand the classifica­tion system of Papile et al. [1] to appropriately categorize a parenchymal hemorrhage not involving the ventricular system, such as grade 4A. We and others [103] have observed this pattern in several infants (fig. 22).

The availability of a readily accessible and accurate method of evaluating for intraventricular/periventricular hemorrhage and ventriculomegaly allows for the design of clinical protocols aimed at evaluating specific problems and potential outcomes, and testing various preventive and therapeutic methods re­lated to intracranial hemorrhage.

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