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Emergency Radiology

, Volume 25, Issue 3, pp 227–234 | Cite as

Imaging of pediatric neurovascular emergencies

  • Yang Tang
  • William C. Goodman
  • Michael D. Maldonado
  • Xinli Du
Review Article

Abstract

Pediatric strokes are rare but critical diagnoses to make in the emergency setting. They are associated with a set of pathologies that are not frequently encountered in the adult population. Some of these diseases have variable clinical presentations and imaging appearance depending on the age of onset and severity of the underlying pathologies. This article reviews the differential diagnoses and noninvasive imaging evaluation of pediatric cerebral ischemic and hemorrhagic diseases.

Keywords

Pediatric Stroke Hemorrhage Arteriopathy Cerebrovenous thrombosis Arteriovenous malformation Aneurysm 

Introduction

Although relatively rare, stroke is an important cause of morbidity and mortality for children, and is associated with significant health care cost. The incidence is estimated at 2–13 per 100,000 person-year, slightly more common than brain tumors in this age group [1]. Pediatric stroke is often under-recognized by the clinical providers because the clinical presentations are often nonspecific and can be easily confused with other diagnoses such as seizure, infection, or tumor, etc.

CT- and MRI-based noninvasive imaging techniques have been increasingly utilized in the emergency setting, not only to make the diagnosis of strokes, but to reveal the underlying vascular pathologies and guide potential neuro-interventions. Non-contrast CT (NCCT) of the head is typically the first modality to evaluate pediatric neurological emergencies since it is readily available, can be performed quickly, and without the need of sedation. CT angiography (CTA) and CT perfusion are excellent modalities to evaluate the cervical and intracranial vasculatures, and associated cerebral perfusion defects especially in the setting of acute ischemic stroke. The disadvantages of CT include its low sensitivity to detect ischemia within the first few hours of stroke onset, and the risk associated with ionizing radiation, which is particularly a concern for children. Compared to CT, MRI is better with tissue characterization and requires no ionizing radiation. MR angiography (MRA), venography (MRV), and perfusion can be used in conjunction with conventional MRI sequences to evaluate vascular anomalies and associated perfusion changes. However, the limited availability of MRI and the need of sedation for young children have restricted its use in the emergency setting. In addition, time of flight (TOF) MRA and MRV are susceptible to turbulence or in-plane flow artifacts. Catheter angiography is being utilized much less frequently for routine diagnosis and is mainly reserved for diagnosing complex vascular malformations and endovascular treatment planning.

As in adults, pediatric strokes can be either ischemic or hemorrhagic. However, the risk factors are mostly different from those of adults, as atherosclerosis, diabetes, and hypertension are rare in the pediatric population. Instead, pathological entities such as cerebral arteriopathy, congenital heart disease, and vascular malformations are more prevalent in the pediatric stroke patients. In particular, hypoxic–ischemic encephalopathy, inborn errors of metabolism, cerebrovenous thrombosis, and Vein of Galen Aneurysmal Malformation are more commonly encountered in the neonatal period. In this article, we aim to discuss the differential considerations and imaging patterns of neurovascular diseases that are commonly associated with pediatric cerebral ischemia and intracranial hemorrhage (ICH).

Arteriopathy versus cardioembolism

Cerebral arteriopathy is the most common cause of childhood ischemic stroke, and a strong predictor of stroke recurrence and poor short-term outcome [2]. It is defined as an in situ arterial abnormality on vascular imaging, not attributable to cardioembolism or a congenital variant [3]. Broadly speaking, arteriopathy includes focal cerebral arteriopathy (FCA), dissection, moyamoya disease, sickle cell arteriopathy, postvaricella arteriopathy, vasculitis, or other specific diagnoses such as post-irradiation arteriopathy. Among these many entities, FCA is the most common subtype and is thought to be associated with recent upper respiratory infection [2] (Fig. 1).
Fig. 1

Focal cerebral arteriopathy. Eight-month-old baby with seizure like activity of the right arms and legs. a DWI shows acute or subacute infarction in the left basal ganglia and cerebral hemisphere. b Time of Flight (TOF) MRA demonstrates focal stenosis at the origin of the left middle cerebral artery (MCA) (arrow)

Distinguishing arteriopathy from cardioembolism can be challenging even for experienced radiologists, and the distinction should be made by combining the clinical history and imaging findings. The presence of congenital or acquired heart disease, involvement of multiple vascular territories, and abrupt arterial occlusion strongly favor cardioembolic source (Fig. 2), while arterial stenosis or irregularity is more suggestive of underlying arteriopathy.
Fig. 2

Cardioembolic stroke. Seventeen-year-old with history of rheumatic heart disease and mitral and aortic valve replacement presented with acute onset right hemiparesis. a CTA maximum intensity projection (MIP) image shows abrupt occlusion of the distal M1 segment of the left MCA. CT perfusion color maps show prolongation of time to drain (b), and minimally decreased cerebral blood volume (c) of the left MCA territory, consistent with tissue at ischemic risk. The patient underwent emergent mechanical embolectomy. The postprocedural MRI demonstrates minimal infarction (not shown)

In the past, this distinction may not be as critical for emergent management, since the treatment of ischemic stroke in children has mainly been focused on the management of underlying causes and prevention of future events. However, with multiple recent successful endovascular stroke trials in adults, it is likely that endovascular mechanical thrombectomy will play an increasing role in the treatment of a subset of pediatric stroke patients with proximal large vessel occlusion, small infarctions, and large amount of tissue at ischemic risk [4]. In this context, timely and accurate interpretation of CTA/MRA and perfusion imaging has become essential in selecting this group of patients.

Dissection

Arterial dissection is a rare albeit important cause of stroke in the younger population. It can be due to trauma or occur spontaneously in patients with predisposing arterial defects such as fibromuscular dysplasia or connective tissue diseases. It usually arises from an intimal tear, which allows the blood of arterial pressure to enter the arterial wall and form an intramural hematoma or false lumen. Subintimal dissection typically causes luminal stenosis/occlusion, while subadventitial dissection can result in pseudoaneurysms or arterial rupture [5]. The most common clinical presentation is ischemic stroke or transient ischemic attack (TIA), which are due to artery to artery embolization from the dissection rather than cerebral hypoperfusion [6]. Intramural hematoma from internal carotid dissection may also cause a mass effect on surrounding structures, leading to Horner syndrome. Intracranial dissection can occasionally result in subarachnoid hemorrhage.

The extracranial segments of the carotid and vertebral arteries, especially at the skull base, are more susceptible to dissection than the intracranial segments, although cervical dissection can sometime extend intracranially. On cross-sectional imaging, the dissection can manifest as crescent-shaped wall thickening, intimal flap, vascular stenosis, occlusion, or pseudoaneurysms (Fig. 3a). MRI/MRA can directly image the intramural hematoma and resultant cerebral infarction. On MRI, subacute intramural hematoma is typically seen as T1 hyperintense signal that eccentrically or circumferentially narrows the lumen (Fig. 3b). CTA can also show the intramural hematoma as mural hyperdensity, although it may not be easily discernable in subtle cases when the lumen is not significantly compromised.
Fig. 3

Carotid dissection. Fifteen-year old presented with left side weakness after motor vehicle collision. a Sagittal MIP image of CTA demonstrates tapered occlusion of the right cervical ICA due to compression of intramural hematoma (arrow). b Fourteen-year old with spontaneous dissection of the right ICA at the skull base with no history of trauma or other inciting factors. Axial T1 image demonstrates a subacute hyperintense intramural hematoma (arrow)

Moyamoya disease

Moyamoya disease (MMD) is a unique cerebrovascular disease characterized by progressive stenosis of distal intracranial ICAs and collateral network formation around the Circle of Willis. It can be either idiopathic (moyamoya disease) or secondary to conditions such as sickle cell disease, Down syndrome, neurofibromatosis type I, or cranial radiation (moyamoya syndrome) [7]. Ischemic strokes from MMD are more prevalent in children, while hemorrhagic strokes are more common in adults.

On MRI, collateral vessels from the lenticulostriates and thalamoperforators manifest as flow voids in the basilar cisterns and basal ganglia. Bright sulci (so-called leptomeningeal “ivy” sign) may be evident on the FLAIR reflecting slow flow of pial collaterals. Angiographic studies typically demonstrate stenosis/occlusion of distal ICAs and proximal Circle of Willis with collateral formation (Fig. 4). Perfusion studies (SPECT, CT, or MRI perfusion) with Diamox challenge have been used to help identify patients with inadequate cerebral blood flow reserve [8], who may benefit from surgical revasculization such as direct superficial temporal artery to middle cerebral artery bypass or encephaloduroarteriosynangiosis (EDAS).
Fig. 4

MMD. Seventeen-year old with right face and hand paresthesia and weakness. a FLAIR image demonstrates curvilear high signal within the cortical sulci (arrows) consistent with collateral vessels (“ivy sign”). b TOF MRA MIP shows occlusion of the left ICA terminus and left M1 and A1 segments. Stenosis of the right ICA terminus and origins of right A1 and M1 segments are also noted, to a less degree compared to the left. Note numerous lenticulostriate collaterals surrounding the Circle of Willis

CNS vasculitis

CNS vasculitis is characterized by the inflammatory infiltration of the cerebral vessel walls. It encompasses a spectrum of diseases that either manifest as a primary idiopathic brain inflammatory process without other organ involvement (primary angiitis of CNS, PACNS), or occur in the context of CNS infections, systemic rheumatic diseases, or exposure to medications/toxins, etc. PACNS has been increasingly recognized as the most common cause of inflammatory brain disease in childhood [9].

MRI and angiographic studies are essential to establish the diagnosis. MRI is nearly always abnormal in cases of vasculitis but the findings are often nonspecific. The involvement of gray and white matter is similar but there is a strong tendency toward the basal ganglia or lateral lenticulostriate vasculature territory (Fig. 5) [10]. Leptomeningeal or parenchymal enhancement is common. Parenchymal hemorrhage and subarachnoid hemorrhage can also occur in a small percentage of patients [11]. In patients with large or medium vessel vasculitis, vascular studies often reveal findings of stenosis, occlusion, beading, or aneurysms. According to one study, the most common pattern of PACNS in children was unilateral, proximal, multifocal, and supratentorial, and no significant difference was found in the ability of MRA to detect and characterize vasculitis lesions when compared with catheter angiography [10, 12]. High-resolution vessel wall imaging may show wall enhancement in the majority of vasculitis patients and help distinguish it from mimickers such as reversible cerebral vasoconstriction syndrome [13]. It should be noted that sensitivity of angiography is poor for small vessel vasculitis; therefore, a negative angiogram does not exclude this diagnosis. Brain biopsy remains the reference standard, although it is rarely performed in pediatric patients and can be falsely negative if biopsy is performed in the non-lesional areas.
Fig. 5

Vasculitis. Fifteen-year old presented with right side weakness and tingling. FLAIR image demonstrates multiple infarctions of bilateral basal ganglia, some of which are acute with restricted diffusion (not shown) and others are chronic

Hypoxic ischemic encephalopathy

Hypoxic-ischemic encephalopathy (HIE) is a major cause of death and long-term disability in neonates. Potential risk factors for HIE include antepartum, intrapartum, and postpartum factors. Outside the neonatal period, it is mostly associated with nonaccidental trauma, asphyxia, and drowning, etc.

The pattern of neonatal HIE can be either profound (severe) or partial (mild to moderate), depending on the severity and duration of the event. Profound injuries primarily involve the deep gray matter (basal ganglia, ventrolateral thalami, posterior limb of internal capsules, and dorsal brainstem) and occasionally the peri-rolandic cortex, since these areas are actively myelinating and most susceptible to energy depletion. In partial injuries, the cortical/subcortical watershed zones are usually more affected, while the central structures mentioned above are relatively spared due to autoregulation/blood shunting.

The findings on MRI are variable depending on the timing of study. Proton MR spectroscopy is most sensitive during the first 24 h showing a lactate peak. Diffusion restriction is usually evident between day 1 and day 5 but becomes pseudo-normalized after 1 week. Analyzing T1/T2 signals then becomes critical after 1 week. T1 and T2 are frequently normal during the first 24 h. After day 2, T1 hyperintensity occurs in the posterolateral putamina and ventrolateral thalami and can persist in months. T2 is typically hyperintense in these areas during the first week due to edema, then becomes hypointense after the first week. The loss of normal T1 hyperintensity at the posterior limb of internal capsules in a term infant is another sensitive sign for HIE [14].

Cerebrovenous thrombosis

Cerebrovenous thrombosis (CVT) represents an increasingly recognized cause of ischemic and hemorrhagic strokes in pediatric patients, and is the most common cause of symptomatic intraventricular and thalamic hemorrhage in term neonates [15]. Children with CVT, particularly neonates, often present with non-focal neurologic signs and symptoms, and the diagnosis may not be suspected. Many risk factors have been identified, including acute systemic illnesses that are more common in neonates, and local infection adjacent to the dural sinuses, trauma, and prothrombotic conditions that are more common in older children. Deep venous thrombosis more frequently affects the neonates, whereas dural sinus thrombosis occurs more often in the older children [16].

The spectrum of brain injury in CVT ranges from venous congestion, cortical, subcortical and deep gray matter parenchymal infarction and hemorrhage, as well as primary subarachnoid and subdural hemorrhage.

CT or MRI would demonstrate parenchymal edema, infarction, or hemorrhage. Noncontrast CT can show hyperattenuating thrombi in the occluded veins (Fig. 6). On contrast-enhanced CT or MRI, thrombi manifest as filling defects surrounded by contrast (so-called empty delta sign). On MRI, T1 and T2 signal of the thrombi vary depending on the age. The thrombi may show susceptibility on gradient recall echo sequence and high diffusion signal on DWI. The thrombi cause absence of flow-related enhancement in the occluded sinuses or cortical veins on TOF MRV, and are shown as filling defects or lack of enhancement in the occluded veins on contrast-enhanced MRV or CTV. The treatment is anticoagulation, while endovascular mechanical thrombectomy and stenting may be required in severe cases.
Fig. 6

CVT. Newborn with intraventricular and thalamic hemorrhage. Sagittal NCCT image shows hyperdense, thrombosed venous structures including the internal cerebral vein, vein of Galen, straight sinus, and distal portion of the superior sagittal sinus to the torcula (curved arrows), which should not be confused with subdural hemorrhage

Stroke mimickers

A number of disease processes can present with acute neurological deficits and mimic strokes both clinically and on imaging. These include Todd’s paralysis from recent seizure, meningoencephalitis, hemiplegic migraine, and rarely metabolic disorders such as mitochondrial diseases (Fig. 7), organic acidemia, Fabry’s disease, etc. Diffusion restriction and cortical swelling can be seen during the acute phase of these diseases resembling ischemia, although typically do not follow a particular arterial distribution. Careful review of the imaging pattern and correlation with clinical presentation and laboratory tests are essential in making the distinctions.
Fig. 7

Mitochondrial myopathy, encephalopathy, lactic acidosis, stroke-like episodes (MELAS). Ten-year old presented with recurrent strokes and seizures. Axial FLAIR image shows multiple right cerebral cortical infarctions. The right frontal infarction (curved arrow) is acute with corresponding diffusion restriction (not shown), while the infarctions in the lateral and medial right parietal cortices (arrows) are chronic without diffusion abnormality

Vein of Galen aneurysmal malformation

Vein of Galen aneurysmal malformation (VGAM) is the most common congenital arteriovenous shunt. It forms between the intracranial arteries such as choroidal arteries, thalamoperforators, and pericallosal arteries and a midline venous sac, which represents the embryonic prosencephalic vein of Markowski [17]. Two subtypes of VGAM, choroidal and mural types, have been recognized, with the choroidal type being more common and with more severe symptoms. Children with VGAM typically present with cardiac failure, hemorrhage, and seizure.

VGAM can be diagnosed with antenatal or postnatal ultrasound, seen as a hypoechoic or anechoic midline structure with turbulent Doppler flow. On NCCT, it manifests as a hyperdense structure in the quadrigeminal cistern. CTA, MRI, or MRA would show a midline venous varix connected to the dilated straight sinus or fetal falcine sinus, with multiple arterial feeders in the ambient and perimesencephalic cisterns (Fig. 8). Pulsation artifacts associated with high flow can be seen in the phase-coding direction on MRI. MRI is very helpful in delineating the associated hemorrhage, infarction, hydrocephalus, and other brain parenchymal abnormalities that are important for pretreatment counseling.
Fig. 8

VGAM. Sagittal T1 MRI shows a dilated venous pouch at the quadrigeminal cistern with numerous feeders from choroidal arteries and thalamoperforators (arrows), drained into the superior sagittal sinus through a persistent falcine sinus (curved arrow)

Arteriovenous malformation

Pial arteriovenous malformation (AVM) is the most common cause of nontraumatic brain hemorrhage in children. It is a congenital lesion that arises from the abnormal development of a vascular network (nidus) between the arterial and venous circulations. Pial AVMs may be associated with cerebrofacial metameric syndromes as well as genetic conditions such as hemorrhagic hereditary telangiectasia. The most common clinical presentations are intracranial hemorrhage and seizures.

NCCT is useful in detecting acute hemorrhage, mass effect, and hydrocephalus in the context of ruptured AVMs, and may sometimes reveal the tortuous vessels and calcifications associated with the underlying AVMs. MRI more clearly depicts the nidus as a cluster of serpiginous vessels and characterizes its accurate anatomic location, and relationship to adjacent eloquent structures. MRI is also much more sensitive to subacute and chronic hemorrhages. CTA/CTV and MRA/MRV are both excellent noninvasive modalities in mapping the feeding arteries and draining veins (Fig. 9). AVMs are graded with the Spetzler-Martin system by assigning points based on the size of the nidus, eloquence of the involved brain, and venous drainage pattern [18]. Additional angioarchitectural features such as the presence of nidal or flow-related aneurysms, venous pouch, and stenosis of draining veins should also be carefully evaluated when interpreting these vascular studies.
Fig. 9

AVM. Thirteen-year old presented with ICH in the left temporal lobe with adjacent subarachnoid extension. Sagittal MIP of CTA shows a nidus in the left temporal lobe (circle), supplied with the posterior division of the left MCA (white arrow) and with superficial venous drainage into the superior sagittal sinus (black arrow). Note is made of an intranidal aneurysm (curved arrow), which is causative of the acute hemorrhage

Cavernous malformation

Cavernous malformation (CM) is an angiographically occult vascular malformation frequently associated with developmental venous anomalies. It is the second most common cause of spontaneous intracranial hemorrhage in children [19]. Histologically, it consists of hypertrophic vascular channels containing blood of various ages without intervening brain parenchyma.

CT may show a hyperdense mass, usually with calcifications. MRI is the modality of choice and demonstrates variable T1 and T2 signal intensity depending on the age of blood products (Fig. 10). Post-contrast T1 shows mild or absent enhancement. Gradient-recall echo sequence shows characteristic blooming artifacts from the blood products. Mass effect and edema are typically absent unless there is recent hemorrhage or thrombosis.
Fig. 10

Multiple familial CMs. Axial T2 image demonstrates multiple cavernomas in the left frontal lobe and right parietal lobe with heterogenous T2 signal and rims of hemosiderin deposition

Aneurysm

Intracranial aneurysm is a rare but important cause for ICH in children. The pathogenesis is different from that of adults and may be related to underlying genetic abnormality in the arterial tissue. Compared to the adult counterparts, the pediatric cerebral aneurysms are more likely to have fusiform morphology (Fig. 11a), have a higher percentage of giant aneurysm (> 2.5 cm), and more commonly occur distal to the Circle of Willis and in the posterior circulation. In addition, a higher percentage of pediatric aneurysms are mycotic aneurysms secondary to adjacent infections such as sinusitis/mastoiditis (Fig. 11b), or secondary to endocarditis from congenital or rheumatic heart disease. Posttraumatic pseudoaneurysms are also more common in children than adults. Clinically, older children are more likely to present with acute subarachnoid hemorrhage, while children under the age of 5 often do not. Giant aneurysms can present with focal neurological findings due to compression of adjacent structures [20].
Fig. 11

Aneurysm. a 16-year old presented with headache and vertigo. CTA shows a fusiform basilar artery aneurysm (arrow) with mural thrombus (*). b 17-year old with history of meningitis secondary to frontal sinusitis developed frontal intraparenchymal and subarachnoid hemorrhage. CTA sagittal MIP demonstrates a saccular outpouching from the frontopolar branch of the anterior cerebral artery (arrow), consistent with a mycotic aneurysm

On imaging, NCCT shows acute subarachnoid hemorrhage and hydrocephalus. Larger aneurysms can be detected on MRI as abnormal flow voids or focal enhancing lesions on the postcontrast T1. CTA and MRA are the noninvasive modalities of choice to detect, follow up aneurysms, and for treatment planning.

Hemorrhagic tumors

ICH can occasionally be the initial presentation for pediatric brain tumors. Among all tumor subtypes, medulloblastoma-primitive neuroectodermal tumor is most frequently associated with ICH (Fig. 12) [21]. On imaging, the mass can be obscured by the acute hemorrhage. Presence of mass effect and edema disproportionate to the volume of hemorrhage may provide a clue to the underlying neoplasm. Contrast-enhanced studies are often required to make the diagnosis.
Fig. 12

Hemorrhagic tumor. Three-year old presented with headache and lethargy. NCCT shows a mass lesion (*) within the fourth ventricle with hydrocephalus and acute intraventricular hemorrhage

Conclusion

In summary, we have reviewed the etiologies for pediatric ischemic strokes including arteriopathy, cardioembolism, dissection, MMD, vasculitis, HIE, and CVT, as well as the causes for ICH such as vascular malformations, aneurysms, and tumor. It should be kept in mind that some cerebral vasculopathies, for example CVT and MMD, may be causative of both ischemia and ICH. Some entities may have variable clinical and imaging presentations depending on the age of onset and severity of the disease processes. Given the relative low incidence of pediatric strokes, the above discussed diseases are rarely encountered in the daily radiology practices and can be easily misinterpreted. It is essential that emergency radiologists become familiar with these critical pediatric neurovascular emergencies.

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. 1.
    Jordan LC, Hillis AE (2011) Challenges in the diagnosis and treatment of pediatric stroke. Nat Rev Neurol 7(4):199–208.  https://doi.org/10.1038/nrneurol.2011.23 [doi].
  2. 2.
    Fullerton HJ, Wintermark M, Hills NK, Dowling MM, Tan M, Rafay MF, Elkind MS, Barkovich AJ, deVeber GA, Investigators VIPS (2016) Risk of recurrent arterial ischemic stroke in childhood: a prospective international study. Stroke 47(1):53–59.  https://doi.org/10.1161/STROKEAHA.115.011173 [doi].
  3. 3.
    Wintermark M, Hills NK, DeVeber GA, Barkovich AJ, Bernard TJ, Friedman NR, Mackay MT, Kirton A, Zhu G, Leiva-Salinas C et al (2017) Clinical and imaging characteristics of arteriopathy subtypes in children with arterial ischemic stroke: results of the VIPS Study. AJNR Am J Neuroradiol.  https://doi.org/10.3174/ajnr.A5376
  4. 4.
    Satti S, Chen J, Sivapatham T, Jayaraman M, Orbach D (2016) Mechanical thrombectomy for pediatric acute ischemic stroke: review of the literature. J Neurointerv Surg doi: neurintsurg-2016-012320 [pii] Google Scholar
  5. 5.
    Schievink WI (2001) Spontaneous dissection of the carotid and vertebral arteries. N Engl J Med 344(12):898–906.  https://doi.org/10.1056/NEJM200103223441206 [doi].
  6. 6.
    Morel A, Naggara O, Touze E, Raymond J, Mas JL, Meder JF, Oppenheim C (2012) Mechanism of ischemic infarct in spontaneous cervical artery dissection. Stroke 43(5):1354–1361.  https://doi.org/10.1161/STROKEAHA.111.643338 [doi].
  7. 7.
    Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360(12):1226–1237.  https://doi.org/10.1056/NEJMra0804622 [doi].
  8. 8.
    Vagal AS, Leach JL, Fernandez-Ulloa M, Zuccarello M (2009) The acetazolamide challenge: techniques and applications in the evaluation of chronic cerebral ischemia. AJNR Am J Neuroradiol 30(5):876–884.  https://doi.org/10.3174/ajnr.A1538 [doi].
  9. 9.
    Twilt M, Benseler SM (2013) CNS vasculitis in children. Mult Scler Relat Disord 2(3):162–171.  https://doi.org/10.1016/j.msard.2012.11.002 [doi].
  10. 10.
    Aviv RI, Benseler SM, Silverman ED, Tyrrell PN, Deveber G, Tsang LM, Armstrong D (2006) MR imaging and angiography of primary CNS vasculitis of childhood. AJNR Am J Neuroradiol 27:192-199. Doi: 27/1/192 [pii].Google Scholar
  11. 11.
    Gallagher KT, Shaham B, Reiff A, Tournay A, Villablanca JP, Curran J, Nelson MD Jr, Bernstein B, Rawlings DJ (2001) Primary angiitis of the central nervous system in children: 5 cases. J Rheumatol 28(3):616–623PubMedGoogle Scholar
  12. 12.
    Aviv RI, Benseler SM, DeVeber G, Silverman ED, Tyrrell PN, Tsang LM, Armstrong D (2007) Angiography of primary central nervous system angiitis of childhood: conventional angiography versus magnetic resonance angiography at presentation. AJNR Am J Neuroradiol 28:9-15. Doi: 28/1/9 [pii].Google Scholar
  13. 13.
    Obusez EC, Hui F, Hajj-Ali RA, Cerejo R, Calabrese LH, Hammad T, Jones SE (2014) High-resolution MRI vessel wall imaging: spatial and temporal patterns of reversible cerebral vasoconstriction syndrome and central nervous system vasculitis. AJNR Am J Neuroradiol 35(8):1527–1532.  https://doi.org/10.3174/ajnr.A3909 [doi].
  14. 14.
    Huang BY, Castillo M (2008) Hypoxic-ischemic brain injury: imaging findings from birth to adulthood. Radiographics 28:417-39; quiz 617. Doi:  https://doi.org/10.1148/rg.282075066 [doi]
  15. 15.
    YW W, Hamrick SE, Miller SP, Haward MF, Lai MC, Callen PW, Barkovich AJ, Ferriero DM (2003) Intraventricular hemorrhage in term neonates caused by sinovenous thrombosis. Ann Neurol 54:123–126.  https://doi.org/10.1002/ana.10619 [doi].
  16. 16.
    Lolli V, Molinari F, Pruvo JP, Soto Ares G (2016) Radiological and clinical features of cerebral sinovenous thrombosis in newborns and older children. J Neuroradiol 43(4):280–289.  https://doi.org/10.1016/j.neurad.2015.12.001 [doi].
  17. 17.
    Barkovich AJ, Raybaud C (2012) Pediatric neuroimaging. Wolters Kluwer Lippincott Williams & WilkinsGoogle Scholar
  18. 18.
    Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65(4):476–483.  https://doi.org/10.3171/jns.1986.65.4.0476 [doi].
  19. 19.
    Liu AC, Segaren N, Cox TS, Hayward RD, Chong WK, Ganesan V, Saunders DE (2006) Is there a role for magnetic resonance imaging in the evaluation of non-traumatic intraparenchymal haemorrhage in children? Pediatr Radiol 36(9):940–946.  https://doi.org/10.1007/s00247-006-0236-9 [doi].
  20. 20.
    Gemmete JJ, Toma AK, Davagnanam I, Robertson F, Brew S (2013) Pediatric cerebral aneurysms. Neuroimaging Clin N Am 23(4):771–779.  https://doi.org/10.1016/j.nic.2013.03.018 [doi].
  21. 21.
    Laurent JP, Bruce DA, Schut L (1981) Hemorrhagic brain tumors in pediatric patients. Childs Brain 8(4):263–270PubMedGoogle Scholar

Copyright information

© American Society of Emergency Radiology 2018

Authors and Affiliations

  1. 1.Department of RadiologyVirginia Commonwealth University Medical CenterRichmondUSA
  2. 2.Department of Neurology, Hunter Holmes McGuire VA Medical CenterVirginia Commonwealth University Medical CenterRichmondUSA

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