Serial MRI in infantile bilateral striatal necrosis

Serial MRI in Infantile Bilateral Striatal Necrosis Katsutoshi Fujita, MD*, Yoshihiro Takeuchi, MDt, Akira Nishimura, MD*, Hiroshi Takada, MD*, and Tadashi Sawada, MDt A 3-year-old girl with left hemiparesis suffered from bilateral paresis, motor rigidity, gait disturbance, axial hypotonia, dysarthria, apathy, and incontinence. After steroid therapy, mild improvement occurred, but muscle weakness, gait disturbance, and rigidity remained. Leigh encephalopathy was excluded on the basis of muscle biopsy and laboratory findings. Computed tomography and serial magnetic resonance imaging at an early stage revealed right-sided dominant lesions in the putamen and caudate nucleus and later bilateral striatai lesions, appearing as hyperintense signals on T2-weighted images and mixtures of hypo- and hyperintense signals on Tl-weighted images. This is the first demonstration of serial magnetic resonance imaging findings in infantile bilateral striatal necrosis. Fujita K, Takeuchi Y, Nishimura A, Takada H, Sawada T. Serial MRI in infantile bilateral striatal necrosis. Pediatr Neurol 1994; 10:157-160.

atal necrosis (IBSN) to be observed in vivo, and serial studies allow assessment of the evolution of the disease [2-7]. We report a patient with IBSN, providing the first demonstration of serial MRI findings in IBSN from an early stage of the disease. Case Report This 3-year-old girl, the third child of unrelated parents, was born at term after a normal pregnancy. The delivery and postnatal period were uncomplicated. There was no family history of a neurologic disorder. She suffered a febrile illness, diagnosed as pharyngitis. Several days later, her family noticed clumsiness in movement of the left forearm which remained unchanged for 3 weeks. She then was admitted to the Department of Pediatrics, Ohtsu Municipal Hospital. The medical history was not contributory to her illness. Before admission, she suffered from neither convulsions nor disturbed consciousness. Physical examination revealed paresis and rigidity of the left upper extremity, but no pathologic reflexes were observed. Eye movements were full and both optic discs normal. The following tests were normal, including routine hematologic and chemical studies, serum NH3, copper, ceruloplasmin, pyruvate, lactate, arterial blood gases, amino acid, and urinary organic acid analysis. Cerebrospinal fluid (CSF) examination results, including the pyruvate and lactate levels, were normal. No cultural or serologic evidence of any viral infection was detected. Cranial CT revealed multiple low-density areas predominantly in the right basal ganglia, namely the putamen, caudate nucleus, and globus pallidus (Fig 1A). TE-weighted MRI (TR: 2,500 ms, TE: 100 ms) revealed multiple hyperintense areas, as supported by CT (Fig 1B). To eliminate cerebrovascular disease, such as moyamoya disease, cerebral angiography was performed which revealed no abnormalities. She underwent rehabilitation and the left hemiparesis, which appeared predominantly in the upper extremity, improved gradually. She was discharged 1 month after admission. About 3 months later, she suffered from rubella. Soon after she complained of gait disturbance and thus was readmitted for further examination. She had mild hyperreflexia bilaterally, except for the right lower extremity, but no pathologic reflexes were observed. T2-weighted MRI

Introduction Friede, under the term "infantile bilateral striatal necrosis," reviewed the reported childhood cases of bilateral necrosis of the striatum with negligible damage elsewhere in the brain [ 1]. With the development of modem imaging techniques, such as computed tomography (CT) and magnetic resonance imaging (MRI), there has been an increase in reported patients with progressive neurologic deficits beginning in childhood and associated with selective lesions of the basal ganglia. Although they cannot replace neuropathologic examination, these neuroradiologic techniques do enable new patients with infantile bilateral stri-

From the *Department of Pediatrics; Ohtsu Municipal Hospital; Ohtsu, Shiga; tDepartment of Pediatrics; Kyoto Prefectural University of Medicine; Kyoto, Japan.

© 1994 by Elsevier Science Inc. • 0887-8994/94/$7.00

Figure 1. (A) Cranial CT at the basal ganglia on the first admission revealed low-density areas in the left putamen, globus pallidus, right head of the caudate nucleus, and posterior portion of the right putamen. R: right. (B) MRI on the first admission. A T2-weighted image (TR: 2,500 ms, TE: 100 ms) demonstrated hyperintense areas in the same portions as detected on CT in Figure 1A. Other than these areas, patchy hyperintense spots were observed in the anterior portion of the left putamen. R: right.

Communications should be addressed to: Dr. Takeuchi; Department of Pediatrics; Kyoto Prefectural University of Medicine; Kawaramachi-Hirokoji, Kamikyo-ku; Kyoto 602, Japan. Received April 15, 1993; accepted August 30, 1993.

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Figure 2. Serial MRI examinations at the basal ganglia. (A,C,E) T1weighted images (TR: 650 ms, TE: 20 ms). (B,D,F) T2-weighted images (TR: 2,500 ms, TE: 100 ms). (A) Note the patchy appearance of the mixture of hypo- and hyperintense areas in the bilateral putamen. (B) The hyperintense areas in the left putamen had expanded on a T 2weighted image. (C) Hyperintense areas were observed in the right putamen and the posterior portion of the left putamen. (D) The hyperintense areas in the left putamen had increased further in a T2-weighted image, involving the internal and external capsules. (E) Note an additional hyperintense area in the anterior portion of the left putamen. (F) The hyperintense areas had expanded markedly, involving the left caudate nucleus, the putamen, the globus pallidus, and the surrounding white matter, while the sizes of the hyperintense area in the right putamen had decreased.

documented expansion of the hyperintense signals, especially in the left putamen, while the sizes of hyperintense areas had decreased in the right putamen (Fig 2B). Tl-weighted images (TR: 650 ms, TE: 20 ms) demonstrated hypointense signals in the bilateral caudate nucleus and putamen (Fig 2A). It was noteworthy that there were hyperintense signals in the putamen intermingled with hyperintense signals on Tl-weighted images (Fig 2A). Two weeks later, the left caudate nucleus and putamen demonstrated further expansion of the lesions in both T~- and T~weighted images (Figs 2C,2D). Six weeks later the lesions in the left caudate nucleus and putamen had become maximum on T2-weighted images (Fig 2F). A relatively large hyperintense area was observed in the anterior portion of the left putamen (Fig 2E). At this stage, she walked like a patient with Parkinson disease

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Figure 3. Serial MRI examinations at the basal ganglia. ¢A,C.E) T~ weighted images (TR: 650 ms. TE: 20 ms). (B,D,F) T2-weighted images (TR: 2,500 ms, TE: 100 ms J. CA) Hypo- and hyperintense areas present in the bilateral putamen remained. (B I The hyperintense areas in the left putamen had decreased on a T2-weighted image. (C ) Hyperintense areas were observed in the bilateral putamen and the right caudate nucleus. (D) The hyperintense areas in the left puramen had decreased in a T2-weighted image, constituting symmetric striatat lesions compatible with IBSN. (E) Note the persistent hyperin~nse areas in the bilateral putamen and the right caudate nucleus on a Tl-weighted image. ¢FJ The bilateral striatal lesions remained almost unchanged and her countenance was apathetic. She occasionally exhibited intenuon tremor in the right upper extremity. Several weeks later she could neither sit nor roll over and she suffered from dysarthria and urinary incontinence. Mental retardation was unclear. Muscle biopsy was performed, but neither ragged-red fibers nor any other structural abnormality was detected. The results of repeated examinations of the blood and CSF pyruvate and lactate levels were within normal limits. Nerve conduction studies revealed the median nerve (right) to be normal for sensory, motor, and F-wave conduction. Posterior tibial motor nerve conduction was bilaterally within normal limits (42 m/s, right = left). Considering the rapid progress of the neurologic deficits and marked expansion of the basal ganglia lesions documented especially by T zweighted MRI (Fig 2F), [3-methasone was administered orally for about 4 weeks and methylprednisolone pulse therapy for 3 days also was added. One month later, dysarthria and urinary incontinence began to

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disappear slowly, followedby gradual improvementof bilateral paresis and gait disturbance. Within the next severalmonths she could sit alone and soon after was able to walk with support, although the right-sided dominant paresis remained. With gradual improvementof the neurologic findings, the striatal lesions decreased in size (Figs 3A,3B). MRI demonstrated almost completely symmetric lesions in the striatum on T2-weighted images, although mixed hypo- and hyperintense lesions remained bilaterally, as observed in Tl-weightedimages. Four months later, transientworsening of the gait disturbance and right hemiparesis occurred, but the striatal lesions demonstratedby MRI remained unchanged (Figs 3C-3F,4).

Discussion Since its identification by Friede [I], infantile bilateral striatal necrosis (IBSN) rarely has been reported. The clinical features associated with the lesions are variable and include convulsions, disturbed consciousness, apathy, gait disturbance, rigidity, chorea, athetosis, tremor, dystonia, and mental retardation [2]. With the development of noninvasive imaging techniques, there has been an increase in reported patients with IBSN and related conditions [2-7]. The reported patients can be divided into 3 subgroups: (1) Those of definite or probable subacute necrotizing encephalopathy (Leigh disease); (2) Those of familial degeneration of the striatum with an insidious onset and a slow, progressive course; and, (3) Those presenting with abrupt neurologic dysfunction following acute systemic illness [8]. Our patient is considered to belong to the third subgroup. CT and MRI documented selective lesions in the striatum, namely the caudate nucleus and putamen. The differential diagnoses of basal ganglial degeneration in childhood include Wilson disease, juvenile Huntington chorea, carbon monoxide intoxication, status marmoratus, Hailervorden-Spatz disease, Leigh encephalopathy, and IBSN [9]. In our patient, all of these disorders, except for Leigh encephalopathy, can be easily eliminated on the basis of the family history, clinical findings, and laboratory data.

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It has been reported that Leigh encephalopathy encompasses several nosologic entities related to different disorders of energy metabolism, such as mitochondrial encephalopathies [5]. Although the final diagnosis depends on a neuropathologic study, we believe that Leigh disease is unlikely in our patient, judging from the following points; (1) CT and serial MRI revealed no lesions outside the striatum, such as in the brainstem, thalamus, cerebral cortex, or cerebellum; (2) There were no eye movement abnormalities; (3) Blood and CSF levels of lactate and pyruvate were invariably normal; (4) Muscle biopsy revealed no ragged-red fibers; and, (5) The age of onset was older than 3 years of age [5,8,10-13]. Therefore, our patient is considered to have nonhereditary or sporadic IBSN. Sporadic IBSN is induced by a variety of endogenous and exogenous factors, such as intoxication, hypoxia, hyperglycemia, glutamic acidemia, circulatory/respiratory arrest, and infection [3,6,14]. As to the causative agents of infection, mumps and ECHO 25 virus have been reported, but the causative agent is not identified in many patients [3]. In our patient, pharyngitis and rubella are considered to have played roles in initiating or accelerating the course of IBSN. Some reports of MRI findings in IBSN are available [5-7], but few of serial MRI findings from the beginning of the illness. The common MRI finding shared by all reported patients with IBSN is the symmetric Tl-lOw- and T2-high-signal intensity area congruent with the bilateral striatum. At first, we diagnosed our patient as having multiple infarctions produced by some cerebrovascular disease; however, this possibility was eliminated by cerebral angiographic, CT, and serial MRI findings. The most conspicuous serial MRI findings in our patient included the multifocal lesions in the striatum at an early stage and the patchy hyperintense areas on Tl-weighted images which were apparent from an early stage of the illness. These

Fujita et al: Serial MRI in Striatal Necrosis 159

hyperintense areas on Tl-weighted images are considered to reflect astrogliosis, which has been reported neuropathologically to be marked in IBSN, rather than bleeding or fatty tissues. The pathogenesis of IBSN remains unknown, but the high selectiveness of the brain lesions may indicate parainfectious cytotoxic changes, immunologic mechanisms, and latent metabolic disturbances as possible factors. Additional reports of serial MRI findings in combination with neuropathologic studies may clarify these points in the future. We thank Dr. Yasuko Itagaki, Utano National Hospital, for performing the pathologic examination of the muscle biopsy specimens. We also thank Dr. Yasushi Iwasaki, the Department of Radiology, Ohtsu Municipal Hospital, for MRI consultations.

References

[1] Friede RL. Developmental neuropathology. Vienna: SpringerVeflag, 1975;88-9. [2l Roytta M, Olsson I, Sourander P, Svendsen P. Infantile bilateral striatal necrosis: Clinical and morphological report of a case and a review of the literature. Acta Neuropathol 1981 ;55:97-103. [3] YL~tkohehi S, Akabane T, Moil T, Tamagawa K, Morimatsu Y. A case report of infantile striatal necrosis with an acute onset. Brain Dev 1986;8:609-14. [4] Kretzsclmlm- K, Ludwig B, Kramer G, Collmann H, Kazner E. Bilateral lesions of the putamina. Neuroradiology 1986;28:87-91.

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[5] Martin JJ, Van de Vyver FL. Scholte HR, et al. Defect in succinate oxidation by isolated muscle mitochondria in a patient with symmetrical lesions in the basal ganglia. J Neurol Sci 1988;84:189-200. [6l Bruyn GW, Vielvoye GJ, Went LN. Hereditary spastic dystonia: A new mitochondrial encephalopathy? Putaminal necrosis as a d~ agnostic sign. J Neurol Sci 1991;103:195-202. 17] Leuzzi V, Bertini E, De Negri AM, Gallucci M, Garavaglia B. Bilateral striatal necrosis, dystonia, and optic atrophy in two siblings. J Neurol Neurosurg Psychiatry 1992;55:16-9 [8] Gouti6res F, Aicardi J. Acute neurological dysfunction associated with destructive lesions of the basal ganglia in children. Ann Neurol 1982;12:328-32. [9l Mitn T, Tanaka T, Becket LE, Takashima S, Tanaka J. infantile bilateral striatal necrosis: Clinicopathological classification. Arch Neurot 1986;43:677-80. ll0l Koch TK, Yee MHC, Hutchinson HT, Berg BO, Magnetic resonance imaging in subacute necrotizing encephalopathy (Leigh's disease). Ann Neurol 1986;19:605-7. [tl] Davis PC, Hoffman JC, Braun IF, Ahmann P, Krawiecki N. MR of Leigh's disease (subacute necrotizing encephalomyopathy). Am J Neuroradiol 1987;8:71-5. [12] Kissel JT, Kolkin S, Chakeres D, Boesel C, Weiss K. Magnetic resonance imaging in a case of autopsy-proved adult subacute necrotizing encephalomyelopathy (Leigh's disease~. Arch Neurol 1987;44: 563-6. [13] Medina L, Chi TL, De Vino DC, Hilal SK. MR findings in patients with subacute necrotizing encephatomyelopathy (Leigh syndrome): Correlation with biochemical defect. Am J Neuroradiol 1990; 11:379-84. [14] Goodman SI, Norenberg MD. Glutamic acidemia as a cause of striatal necrosis in childhood. Ann Neurol t983;13:582.