Neonatal subpial hemorrhage: clinical presentation, neuroimaging findings and outcome

Abstract

Purpose: Subpial hemorrhage is a rare form of intracranial hemorrhage (ICH) in neonates that remains underreported and inadequately understood. The aim of this study is to characterize the neuroimaging patterns of subpial hemorrhage, assess changes in the underlying brain parenchyma, and examine its clinical features and outcomes.

Methods: We reviewed the medical records and neuroimaging data of neonates with subpial hemorrhage admitted to our hospital between January 2010 and December 2023. Cases of subpial hemorrhages were identified through keywords searches within the hospital´s electronic database.

Results: Twenty-eight patients were included in this retrospective study, 82% of whom were born at term. The most common clinical indication for imaging was a combination of apneas and seizures, ocurring in 50%. Hematologic abnormalities were present in 58% of patients. Magnetic resonance imaging (MRI) was performed acutely at the time of presentation between days 1 and 9 of life in 85% of cases. Subpial hemorrhages were unilateral in 86% of neonates, most commonly located in the temporal lobe (44%), and associated with other type of intracranial hemorrhage in 96% of cases, most often parenchymal (86%) and subdural (64%) hemorrhages. We identified three imaging patterns of subpial hemorrhage and two patterns of changes in the underlying brain parenchyma. Additionally, the hyperintense pia mater sign (HPm-sign) was observed on time-of-flight MR angiography (TOF-MRA) in 12 of 18 patients. Neurologic sequelae were noted in 28% of survivors.

Conclusion: Subpial hemorrhage has a distinctive MR pattern, often accompanied with cortical infarction and in most cases underlying parenchymal hemorrhage. In this study, we identified the HPm-sign that may be used to differentiate subpial hemorrhage from other types of hemorrhages. Additionally, we found a correlation between prominent medullary veins (PMV) and intraparenchymal hemorrhage (IPH).

Keywords: Intracranial hemorrhage; Magnetic Resonance Imaging; Neonatal subpial hemorrhage; Perinatal stroke.

Fig. 1

Patterns of neonatal subpial hemorrhage. Pattern 1. Brain MRI in a 2-day-old term male with apnea and seizures (a-b). Axial T1-weighted (a) and T2-weighted images (b) showing a hematoma with a high signal intensity and low signal intensity respectively along the medial side of the left parietal lobe. Pattern 2. Brain MRI in a 4-day-old term male with apnea, seizure and therapeutic hypothermia for HIE (c-d). Axial T1-weighted (c) and T2-weighted images (d) showing a hematoma with high signal intensity in the left temporal lobe. Pattern 3. Brain MRI in a 7-weeks-old term female with atrioventricular septal defect and pulmonary hypertension (e–f). Axial T2-weighted images (e, f) showing a hematoma with mixed signal intensity in the left temporal lobe

Fig. 2

Neonatal subpial hemorrhage with underlying cortical infarct and small white matter hemorrhage. Brain MRI in a 5-day-old term male with seizures (a-e). Axial T1-weighted image (a) shows high signal intensity, T2-weighted (b) and susceptibility-weighted (c) images show low signal intensity of subpial hemorrhage on left parietal lobe overlying cortex and the precentral gyrus (arrows). Axial DWI (d) and ADC (e) maps show decreased diffusivity indicating underlying cortical infarct (curved arrows). Note small hemorrhage in the underlying white matter (open arrows in a, b, c)

Fig. 3

Neonatal subpial hemorrhage with underlying cortical infarct and large white matter hemorrhage. Brain MRI in a 2-day-old term female with forceps delivery, seizures (a-f). Axial and coronal T1-weighted (a, b) and T2-weighted (c, d) images show high and low signal intensity of a large subpial hemorrhage along the medial aspects of the right frontal/parietal lobes (arrows). Axial DWI (e) and ADC (f) maps shows extensive cytotoxic edema of the underlying cortices (curved arrows). Note large parenchymal hemorrhage in the underlying white matter (open arrows in a, b, c, d)

Fig. 4

Neonatal subpial hemorrhages with Yin-yang sign. Brain MRI in a 1-day-old term male with apneic events and seizures (a-b). Coronal T2-weighted image (a) shows low signal intensity corresponding to subpial hemorrhage splaying underlying sulcus, and DWI (b) shows a bright underlying cerebral cortex with cytotoxic edema of temporal lobe cortical ribbon indicating underlying infarcted brain parenchyma (dotted circles). Brain MRI in a 6-day-old term male with forceps delivery and apnea (c-d). Axial T2-weighted image (c) and DWI (d) show the combination of a dark subpial hemorrhage and a bright underlying cerebral cortex (extensive cytotoxic edema) resembling the yin-yang symbol ( dotted circles)

Fig. 5

Neonatal subpial hemorrhage with the hyperintense pia mater sign. Brain MRI in a 2-old-day term female with apneic events and seizures (a-d). Axial and coronal T2-weighted images (a, b) show a low signal intensity subpial hemorrhage (arrows) splaying underlying sulcus (open arrow) on left frontal lobe separated from CSF (short arrows) with associated subcortical white matter hemorrhage (open arrowheads). Note mass effect. Axial DWI (c) shows cytotoxic edema of right frontal lobe cortical ribbon (curved arrow) due to acute cortical infarction. Axial TOF-MRA (d) demonstrates a linear high signal intensity surrounding the outer contour of subpial hemorrhage, distinctly separated from both cortical ribbon and the subpial hemorrhage indicative of a blood-stained lifted-off pia matter (arrow)

Fig. 6

Neonatal subpial hemorrhage with the hyperintense pia mater sign. Brain MRI in a 3-old-day term male with apnea and seizures (a-f). Axial and coronal T2-weighted images (a, b) show a low signal intensity subpial hemorrhage (arrows) splaying underlying sulcus (open arrow) on right temporal lobe separated from the CSF (short arrows). SWI (c) shows a severe hemorrhage in the underlying white mater (open arrowhead). Axial DWI (d) and ADC (e) maps demonstrate cortical infarct (curved arrows). Axial TOF-MRI (f) demonstrates the HPm-sign (arrow)

Fig. 7

Distribution of concomitant hemorrhages in neonates with subpial hemorhage by location. IPH indicates intraparenchymal hemorrhage; SDH, subdural hematoma; SAH, subarachnoid hemorrhage; IVH, intraventricular hemorrhage; CBH, cerebellar hemorrhage

Fig. 8

Distribution of overlapping hemorrhages neonates with subpial hemorrhage. IPH indicates intraparenchymal hemorrhage; SDH, subdural hematoma; SAH, subarachnoid hemorrhage; IVH, intraventricular hemorrhage; CBH, cerebellar hemorrhage