Magnetic Resonance Angiography of Primary Varicella Vasculitis: Report of Two Cases
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1 JOURNAL OF MAGNETIC RESONANCE IMAGING 9: (1999) Clinical Note Magnetic Resonance Angiography of Primary Varicella Vasculitis: Report of Two Cases Larry A. Kramer, MD, 1 * Carlos Villar-Cordova, MD, 2,3 James W. Wheless, MD, 2,3 John Slopis, MD, 2,3 and Joel Yeakley, MD 1 Two patients with onset of hemiparesis 3 weeks following primary varicella infection demonstrated contralateral temporal lobe and basal ganglia infarctions on magnetic resonance imaging. In both cases, magnetic resonance angiography (MRA) was performed and demonstrated flow abnormalities ipsilateral to the infarcts. Digital subtraction angiography was performed in one case; however, the findings were significantly less conspicuous than those of the MRA. MRA proved to be sensitive to the diagnosis of varicella-induced vasculitis in two consecutive cases and provided a noninvasive means of following the progression of the disease process in response to therapy. J. Magn. Reson. Imaging 1999;9: Wiley-Liss, Inc. Index terms: basal ganglia; infarction; vasculitis; varicella; viruses; MRA; MRI; central nervous system; children 1 Department of Radiology, The University of Texas Houston Medical School, Houston, Texas Department of Neurology, The University of Texas Houston Medical School, Houston, Texas Department of Pediatrics, The University of Texas Houston Medical School, Houston, Texas *Address reprint requests to: L.A.K., UTHSC-Houston, Department of Radiology, Medical School, 6431 Fannin, MSB, Houston, TX Received March 5, 1998; Accepted August 3, Wiley-Liss, Inc. 491 PRIMARY VARICELLA ZOSTER VIRUS infections (chickenpox) that involve the central nervous system (CNS) have an observed incidence ranging from 0.1% to 0.75% (1). Nervous system complications of varicella are well known and include cerebellar ataxia, meningoencephalitis, aseptic meningitis, polyradiculoneuropathy, optic neuritis, transverse myelitis, and Reyes syndrome (2,3). A less common sequela of varicella is CNS vasculitis, leading to the development of basal ganglia infarction and hemiplegia (4). Since acute hemiplegia of childhood has multiple etiologies (3), a thorough work-up is always required including laboratory and neuroimaging studies. MRI is sensitive in detecting both cortical and sub-cortical ischemic areas (5); however, confirmation of a vasculitic process often requires an arteriogram with its consequent risk. We report on two cases that presented with delayed hemiparesis following a primary varicella infection whose lesions were accurately diagnosed with magnetic resonance angiography (MRA). In one of the cases, a follow-up MRA showed interval resolution of the radiographic abnormalities. CASE REPORTS Patient 1 Three weeks after resolution of well-documented chickenpox infection, a previously healthy 2-year-old boy presented with acute onset of left hemiparesis and left homonymous hemianopsia. His physical exam revealed no active skin lesions; however, there were healing pox marks. Neurologically, he was fully awake and playful. Cranial nerve findings were significant for a left visual field cut and a left central facial paresis. His left-sided weakness affected the arm and face more than the leg. Sensory exam was normal. A left Babinski sign was present. All laboratory studies including a complete blood count, electrolytes, liver function tests, coagulation profile, erythrocyte sedimentation rate, and antinuclear and antiphospholipid antibodies were negative except for varicella-zoster Ab titers, which were positive at 1:2048. A lumbar puncture revealed 5 white blood cells (WBC)/mm 3, 580 red blood cells (RBC)/mm 3, protein of 27 mg/dl, and glucose of 69 mg/dl. Electroencephalography (EEG) showed focal slowing over the right hemisphere. MRI of the brain and MRA of the carotid arteries and intracerebral circulation were obtained 2 days after admission using a 1.5 T magnet. A T2-weighted [TR 2000 msec, TE 80 msec, field of view (FOV) 22, matrix, number of excitations (NEX) 1] conventional spin-echo axial image was obtained that demonstrated increased signal intensity in the right putamen and temporal lobe (Fig. 1A). A three-dimensional (3D) phase contrast MRA (TR 24 msec, TE 7.2 msec, FV 40 cm/se, FOV 22, matrix, 1 NEX) gradientecho image was obtained and demonstrated narrowing of the right M1 and A1 segments of the cerebral arteries (Fig. 2A). The MRI and MRA studies were repeated after 6 weeks and revealed normalization of flow in the M1 and A1. Chronic infarcts of the right temporal lobe, frontal lobe, putamen, and caudate nucleus were also noted (Figs. 1B, 2B).
2 492 Kramer et al. Figure 1. A: Axial T2-weighted image at the level of the lateral ventricles obtained 2 days after admission demonstrates increased signal in the right putamen, insular cortex, and posterior temporal cortex compatible with an acute vascular insult. B: Six weeks later a repeat T2-weighted image at the level of the lateral ventricles demonstrates gliosis and atrophy of the right putamen and caudate head. Note the enlargement of the right frontal horn. There is atrophy of the right frontal, insular, and posterior temporal cortex and gliosis of the adjacent subcortical white matter. The patient was treated with acyclovir, Solu-Medrol, and aspirin. A follow-up clinical exam revealed residual mild left-sided weakness. Patient 2 A 6-year-old white boy presented to a local emergency room with alternating hemiparesis. Initially, he suffered from an episode of left-sided weakness affecting the arm and leg that lasted about 20 minutes and then resolved. Minutes later he developed a fluctuating right hemiparesis for another 30 minutes. The deficit eventually improved, and he was left with a mild right facial weakness. The remainder of his physical exam was normal. Past medical history was unremarkable except for a recent eruptive varicella infection 3 weeks previously. He had normal developmental milestones. On admission, he was started on Solu-Medrol and acyclovir. EEG revealed abnormal focal slowing in the form of polymorphic delta activity over the left posterior quadrant. His initial lab work revealed a moderate leukocytosis and normal electrolyte, serum lactate, pyruvate, and ammonia levels. Cerebrospinal fluid (CSF) examination showed a protein of 25 mg%, a glucose of 58%, and 1 WBC with no RBCs. His varicella-zoster Ab titers were positive at 1:512. MRI of the brain was obtained on admission using a 1.5 T magnet. In addition, because of concerns of large vessel thrombosis and the potential need for anticoagulation, MRA of the carotid arteries and intracerebral circulation was also obtained. T2-weighted (TR 2000 msec, TE 80 msec, FOV 24, matrix, 1 NEX) conventional spin-echo and fast fluid-attenuated inversion-recovery (FLAIR) (TR 10,000 msec, TE 128 msec, TI 1000 msec, FOV 24, matrix, 2 NEX) axial views were obtained that demonstrated increased signal intensity in the left anterior caudate nucleus, putamen, and insular cortex (Fig. 3A,B). A 3D time-of-flight (TOF) MRA (TR 50 msec, TE 6.9 msec, FA 25, FOV 22, matrix, 1 NEX) spoiled gradient-echo image and a 3D phase contrast MRA (TR 24 msec, TE 7.2 msec, FV 40 cm/sec, FOV 24, matrix, 1 NEX) gradientecho image were obtained. The MRA sequences demonstrated narrowing of the left supraclinoid carotid artery and left M1 segment (Fig. 3C,D). The phase contrast MRA also demonstrated diminished flow in the left middle cerebral artery (Fig. 3C). Heparin therapy was
3 MRA of Primary Varicella Vasculitis 493 Figure 2. A: 3D phase contrast MRA of the carotid arteries and intracranial circulation obtained 2 days after admission reveals diminished signal in the right M1 (large arrow) and A1 segments (small arrow). B: 3D phase contrast MRA of the carotid arteries and intracranial circulation obtained 6 weeks after admission reveals normalized signal in the right M1 (large arrow) and A1 segments (small arrow). initiated to prevent thrombotic occlusion in these regions. The MRA sequences were repeated 8 days later; no significant interval change was seen. Three days later a four-vessel digital subtraction angiogram (DSA) was performed that revealed a subtle narrowing of the left supraclinoid carotid and subtle serrations of the undersurface of the left M1 segment (Fig. 4). The remainder of the intracranial circulation was normal. The patient was discharged 10 days after admission on aspirin 75 mg/day and a tapering dose of steroids. No focal deficits were present on exam. Five months later repeat MRA sequences demonstrated persistent narrowing of the left supraclinoid carotid and left M1 segment, as well as diminished flow in the left middle cerebral artery branches (unchanged from the initial study). The repeat MRI study demonstrated chronic infarction of the left insular cortex, putamen, and caudate nucleus. DISCUSSION Patients with delayed hemiparesis following primary varicella infection have a fairly distinct clinical picture. Typically, neurological symptoms present 3 8 weeks after the viral infection, although the onset may be delayed for up to 4 months. The hemiparesis develops acutely and is usually complete by the time patients are evaluated, although a few cases have shown a stuttering course, and a few have been preceded by transient ischemic attacks. Occasionally, headache, lethargy, and seizures may be also noted. The absence of cortical findings on clinical exam in most cases is supported by imaging data. Computed tomography and MRI demonstrate a preponderance of ischemic infarcts affecting the basal ganglia and the internal capsule, with lessor involvement of the cortex (Table 1). Cortical involvement, which was identified in both of our cases, may in part reflect increased sensitivity of current imaging sequences. In particular, FLAIR sequences, as utilized in Case 2, have been shown to be sensitive to subtle changes in cortical edema (6). Slightly less than half of the cases reported in the literature have undergone cerebral angiography (Table 1). The most common angiographic features are focal narrowing of the proximal segments of the middle and the anterior cerebral arteries. Less commonly, the com-
4 494 Kramer et al. Figure 3
5 MRA of Primary Varicella Vasculitis 495 Table 1 Radiographic Findings of Varicella Vasculitis by Angiogram, MRA, and MRI/CT* Figure 4. Digital subtraction cerebral angiogram with 1024 matrix obtained 8 days after MRI/MRA study. AP projection of the left carotid injection reveals narrowing in the left supraclinoid carotid artery and subtle serrations on the undersurface of the M1 segment (arrows). The middle cerebral and anterior cerebral anterior are not definitely narrowed. mon carotid and basilar artery are involved. At least 4 angiograms have been reported normal out of 14 studies. MRA studies obtained before and after the angiogram in Case 2 demonstrated conspicuous flow abnormalities of the intracranial vessels compared with the more subtle abnormalities identified on the corresponding DSA. Although steroids were started shortly after admission and could account for improvement at the time of the DSA, the follow-up MRA study also obtained after steroid therapy showed persistent conspicuous abnormalities. Case 1, in addition to a reported case of herpes zoster vasculitis secondary to herpes zoster ophthalmicus (7), also demonstrated conspicuous MRA abnormalities; however, no comparative angiograms were performed in either of these cases. The pathogenesis of vasculitis due to herpes zoster virus (HVZ) has been well documented. Herpes virus has been recovered from human brain cells and the Figure 3. A: T2-weighted axial at the level of the lateral ventricles reveals increased signal intensity in the left anterior caudate nucleus, putamen, and insular cortex (arrows). B: Fast FLAIR axial image at the level of the lateral ventricles demonstrates more conspicuous increased signal intensity in the left insular cortex and caudate nucleus (arrows). C: 3D phase contrast MRA coronal sequence through the carotid and intracranial circulation reveals attenuated signal in the left supraclinoid carotid (arrow) and middle cerebral arteries. Normal signal is demonstrated in the right middle cerebral artery and branches. D: 3D TOF axial sequence obtained through the intracranial circulation reveals an attenuated left M1 segment (arrow). Reference Sarazin et al (7) Bodensteiner et al (9) Caekebeke et al (10) Kamholz and Tremblay (13) Silverstein and Brunberg (4) Inagaki et al (14) No. of patients Angiogram Findings MRA Infarcts MRI/CT 1 Severe stenosis of left ACA and MCA, focal stenosis of PCA Left BG, caudate, thalamus, frontal lobe 5 2 normal 1 beading, segmental narrowing of MCA 1 Irregular narrowing of proximal left M1 and basilar 1 Marked stenosis of right M1 and A1 2 1 normal 1 mild narrowing of distal left common carotid, A1 and M1 9 3 narrowing of MCA 6 Eda et al (3) 4 1 normal 3 Liu and Holmes (15) Tsolia et al (2) trigeminal ganglion cells. HVZ antigen has also been found in the CSF of patients with neurologic symptoms and HVZ infection. The trigeminal nerve innervates the proximal middle cerebral and posterior cerebral artery and most likely transmits the virus directly to the vessel. (8) A delayed vasculopathy may also be due to an 4 BG and IC 1 Cortex Left temporal lobe Right BG and centrum semiovale 1 left putamen 1leftGP, putamen, and caudate 2 BG 2 BG, IC, CR 5 1 right IC 1 right IC and putamen 1 left IC and BG 1 left IC and putamen 1 Right putamen, caudate, and IC 1 Left thalamus, left temporal, right temporooccipital cerebellar vermis *BG basal ganglia, IC internal capsule, not done, CR corona radiata; ACA, anterior cerebral artery; MCA, middle cerebral artery; PCA, posterior cerebral artery; GP, globus pallidus.
6 496 Kramer et al. autoimmune phenomenon induced by circulating immune complexes. (9). The prognosis is invariably good, with most cases experiencing complete or nearly complete resolution of their symptoms. One patient reported by Caekebeke et al (10) suffered recurrent hemiparesis 3 and 9 months after a primary varicella infection; both episodes resolved completely. Signal intensity on phase contrast and TOF MRA is not only proportional to blood flow velocity, but is also sensitive to intravoxel spin dephasing due to complex or turbulent blood flow, resulting in reduction in signal intensity at the level of flow disturbance. This phenomenon can result in overestimation of the degree of vascular stenosis (11). This, however, may be advantageous in the evaluation of vasculitis, for which the estimated sensitivity of angiography is only 70% (12). Subtle abnormalities in the luminal diameter and intimal surface topography caused by vasculitis may cause alterations in laminar flow and velocity more readily detectable with MRA. Although the DSA was less conspicuous than the MRA, its increased spatial resolution and lack of intravoxel spin dephasing permitted improved visualization of fine vascular abnormalities not appreciated with the MRA techniques. DSA, therefore, has the potential to provide more specific information regarding the vascular abnormality compared with MRA. CONCLUSIONS HVZ can cause a vasculitis in either primary or secondary infections resulting in neurologic complications. The two patients presented here developed hemiplegia 3 months after a well-documented primary varicella infection. In each case, vasculitis was diagnosed and followed noninvasively by MRA, which was utilized to determine whether to initiate anticoagulation in addition to steroids and acyclovir. Although only one of the patients was evaluated with conventional angiography, this technique demonstrated decreased sensitivity compared with MRA. The possibility that MRA may be inherently sensitive to varicella induced by vasculitis because of alterations in blood flow dynamics not readily detected by angiography is suggested. Further studies, however, will be necessary to confirm this hypothesis. REFERENCES 1. Barnes DW, Whitley, RJ. CNS diseases associated with varicella zoster virus and herpes simplex virus infection. Pathogenesis and current therapy. Neurol Clin 1986;4: Tsolia M, Skardoutsou A, Tsolas G, Karayanni C, Spyridis P, Sinaniotis C. Pre-eruptive neurologic manifestations associated with multiple cerebral infarcts in varicella. Pediatr Neurol 1995;12: Eda I, Takashima S, Takeshita K. Acute hemiplegia with lacunar infarct after varicella infection in childhood. Brain Dev 1983;5: Silverstein FS, Brunberg JA. Postvaricella basal ganglia infarction in children. AJNR 1995;16: Darling CE, Larsen MB, Byrd SE, Radkowski MA, Palka PS, Allen ED. MR and CT imaging patterns in post-varicella encephalitis. Pediatr Radiol 1995;25: Alexander JA, Sheppard S, Davis PC, Salverda P. Adult cerebrovascular disease: role of modified rapid fluid-attenuated inversionrecovery sequences. AJNR 1996;17: Sarazin L, Duong H, Bourgouin PM, et al. Herpes zoster vasculitis: demonstration by MR angiography. J Comput Assist Tomogr 1995; 9: Hilt DC, Buchholz D, Krumholz A, Weiss H, Wolinsky JS. Herpes zoster ophthalmicus and delayed contralateral hemiparesis caused by cerebral angiitis: diagnosis and management approaches. Ann Neurol 1983;14: Bodensteiner JB, Hille MR, Riggs JE. Clinical features of vascular thrombosis following varicella. Am J Dis Child 1992;146: Caekebeke JFV, Peters ACB, Vandvik B, Brouwer OF, de Bakker HM. Cerebral vasculopathy associated with primary varicella infection. Arch Neurol 1990;47: Dumoulin C. Phase-contrast magnetic resonance angiography. Neuroimaging Clin N Am 1992;2: Harris KG, Yuh WT. Intracranial vasculitis. Neuroimaging Clin N Am 1994;4: Kamholz J, Tremblay G. Chickenpox with delayed contralateral hemiparesis caused by cerebral angiitis. Ann Neurol 1985;18: Inagaki M, Koeda T, Takeshita K. Prognosis and MRI after ischemic stroke of the basal ganglia. Pediatr Neurol 1992;8: Liu GT, Holmes GL. Varicella with delayed contralateral hemiparesis detected by MRI. Pediatr Neurol 1990;6:
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