On coronal and sagittal planes, images of various angles were obtained by tilting the microconvex (5–8 MHz) and high-frequency (10–12 MHz) linear transducers through the fontanelles (anterior, posterior, sphenoid, and mastoid). The anterior fontanelle, the largest fontanelle at the junction of the coronal and sagittal sutures, is the optimal sonic window for the supratentorial structures. The mastoid fontanelle is suitable for evaluating the posterior fossa, such as the cerebellum. The American Academy of Pediatrics (AAP) recommended that cUS screening include the anterior fontanelle and the mastoid fontanelle [15]. High-frequency linear transducers provide detailed visualization of the brain and better resolution, which helps evaluate GM-IVH and brain parenchymal lesions. Usually, we recognize the presence of GM-IVH on coronal scans and determine the amount of hemorrhage on parasagittal scans. Doppler images are obtained through the anterior fontanelle using the anterior cerebral artery in the sagittal plane or the middle cerebral artery in the coronal plane [21]. Pulsed wave Doppler US showed peak systolic velocity (PSV), end-diastolic velocity (EDV), and resistive index (RI; PSV−EDV/PSV), which represent intracranial hemodynamics. The average RI declines with GA, and 0.6–0.9 can be used as the normal range for both term and premature infants [33].

GM is most prominent at the caudothalamic groove, which is the most common site of germinal matrix hemorrhage (GMH), from 28 to 32 weeks. The precursor cells in the GM show exuberant proliferation until 28 weeks of gestation, then rapidly decline and involute almost completely by approximately 36 weeks. In premature infants, most cases of GM-IVH occur within the first 3 days after birth. Approximately 95% of GM-IVH cases occur within 7 days. There are some guidelines for screening cUS in premature infants [7,13,15,22].

The AAP recommends cUS for screening and serial evaluation of GM-IVH and periventricular leukomalacia in premature (<30 weeks gestation or >30 weeks gestation with significant risk factors) and VLBW infants [15]. They recommend an initial screening cUS within 7 days. Repeat screening cUS is recommended at 4–6 weeks of age to identify PVL and at TEA or before discharge to determine the permanent effect of brain injury, which can be related to adverse neurodevelopmental outcomes in premature infants.

The most used grading system for GM-IVH (Table 1) was reported in 1978 by Papile et al. [25], which was based on computed tomography; however, it is no longer the recommended imaging modality for premature infants owing to ionizing radiation. In the Papile system, grade I was defined as subependymal hemorrhage, grade II as IVH without ventricular dilatation, grade III as IVH with ventricular dilatation, and grade IV as IVH with parenchymal hemorrhage. Based on the understanding of the drainage of the medullary vein in the deep white matter, parenchymal hemorrhage is considered periventricular hemorrhagic infarction (PVHI) owing to impaired venous drainage and not a parenchymal extension of IVH [30].

The Papile system was adapted by Volpe in 2008 on the basis of US findings, including the presence of GM-IVH and the amount of blood in the lateral ventricles (Table 1) [33]. In the Volpe system, grade I was defined as GMH with no or minimal IVH (<10% of the ventricular area on parasagittal view), grade II as IVH occupying 10% to 50% of the ventricular area in the parasagittal view, grade III as IVH occupying >50% of the ventricular area on parasagittal view with usually distending the lateral ventricle, and the separate notation of periventricular echodensity (location and extent). Periventricular echodensity (i.e., PVHI) can occur in any grade (I–III) of GM-IVH. However, because PVHI is usually accompanied by severe GM-IVH (grade III), most reports continue to use the term “grade IV” GM-IVH in the presence of PVHI, according to the Papile system.

Grade I hemorrhage restricted to the subependymal germinal matrix typically shows a hyperechoic globular lesion located in the caudothalamic groove (Fig. 1A and B) [8,27,29]. Over time, the hematoma becomes heterogeneous and undergoes cystic changes (Fig. 2A and B). The recognition of minimal IVH using cUS is still challenging.

Grade II hemorrhage is IVH without ventricular dilatation (Fig. 1C and D). If the echogenic lesions are anterior to the caudothalamic groove or at the dependent portion of the occipital horns, this suggests IVH [29]. The choroid plexus does not extend into the frontal or occipital horns passing the atrium [20]. The echogenic wall of the ventricle, owing to proliferating subependymal glial cells approximately 1 week after GMIVH, is an indirect sign suggestive of GM-IVH, which might help identify mild GM-IVH (grades I and II) [11].

In grade III hemorrhage, cUS shows ventricular dilatation due to IVH (Fig. 1E and F). Progressive ventricular dilatation after grade II GM-IVH should not be considered grade III [17,27]. We now understand that parenchymal hemorrhage in grade IV GM-IVH of the Papile system is PVHI rather than a parenchymal extension of the hemorrhage [30,33]. It is usually a unilateral, triangular, or “fan-shaped” periventricular echodensity associated with ipsilateral GM-IVH (Fig. 1G and H). Periventricular hemorrhagic infarction can evolve into a porencephalic cyst that often communicates with the adjacent lateral ventricle (Fig. 3).

There are numerous methods for the measurement of the lateral ventricles using cUS (Fig. 6). The ventricular index (VI) and anterior horn width (AHW) are commonly used measurements that showed good intra- and inter-observer agreements [19]. Both measurements were performed using a coronal scan. The VI is the distance between the falx and lateral border of the anterior horn at the level of the foramen of Monro. The AHW is the widest diagonal width of the anterior horn. Another measurement is the thalamo-occipital distance (TOD), which is assessed in the parasagittal scan. The thalamo-occipital distance is the distance between the thalamus and the occipital horn; it has additional value because occipital horn dilatation often precedes frontal horn dilatation. Although normal and cut-off values of variable ventricular measurements have been reported, it is unclear which ventricular measurement in cUS best represents an increase in intracranial pressure (ICP) [2,3].

Recognition of PHVD is the first step in management. Early identification and quantification of ventricular dilatation using serial cUS are necessary after GM-IVH because ventricular dilatation often precedes clinical symptoms and signs of increased ICP. Frequent follow-up cUS after GM-IVH is recommended at least weekly or more than twice a week until resolution of IVH and stabilization of ventricular dilatation [13,15,33].

In a recently reported framework for managing PHVD, ventricular measurements, including VI, AHW, and TOD, are used as key criteria for risk stratification [10]. In the ELVIS trial (Early vs. Late Ventricular Intervention Study) which included premature infants (≤34 weeks) with progressive PHVD after severe IVH, ventricular measurements were used to determine the threshold that determines the timing of treatment (low threshold : VI >97th percentile and AHW >6 mm and/or TOD >25 mm; and high threshold : VI >97th percentile + 4 mm and AHW >10 mm) [5,6].

In addition to ventricular measurements, RI obtained from pulsed-wave Doppler US could provide important information for treatment decisions. An elevated RI indicates an increased ICP, which may require neurosurgical intervention for PHVD [21]. However, because PDA is a common cause of increased RI, caution is needed in interpreting RI in premature infants.

There is still controversy about when and what type of surgical treatment is needed. A recent randomized controlled trial showed that early intervention with reduced ventricular dilatation could improve neurodevelopmental outcomes [6]. Posthemorrhagic ventricular dilatation can be managed with various neurosurgical procedures: lumbar puncture, ventricular drainage, ventriculoperitoneal shunt, and external third ventriculostomy. We can estimate the effect of treatments by performing serial cUS (Fig. 7).