Childs Nerv Syst (2008) 24:269–273 DOI 10.1007/s00381-007-0447-x
CASE REPORT
Appearance of focal cortical dysplasia on serial MRI after maturation of myelination Fumiaki Yoshida & Takato Morioka & Kimiaki Hashiguchi & Yasushi Miyagi & Shinji Nagata & Yui Yamaguchi & Masaharu Ohfu & Tomio Sasaki
Received: 16 May 2007 / Revised: 21 June 2007 / Published online: 7 August 2007 # Springer-Verlag 2007
Abstract Case report It is well known that magnetic resonance imaging (MRI) findings of focal cortical dysplasia (FCD) can change with maturation of myelination. In this paper, we report a patient with intractable epilepsy and negative MRI at the age of 2.5 years, after completion of myelination. Follow-up MRI at the age of 6 years revealed typical FCD findings in the right frontal lobe. During these 3.5 years, electroencephalogram (EEG) consistently depicted an area of irritation in accordance with de novo MRI findings. Intraoperative electrocorticogram showed frequent paroxysmal activity in the right frontal lobe; excision of the epileptogenic cortex resulted in a reduction in seizures. Conclusion It is possible that FCD becomes apparent on MRI even after maturation of myelination; thus, repeated MRI is recommended while EEG continues to demonstrate focal findings.
F. Yoshida : T. Morioka (*) : K. Hashiguchi : Y. Miyagi : S. Nagata : T. Sasaki Department of Neurosurgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-ku, Fukuoka 812-8582, Japan e-mail:
[email protected]
Keywords Focal cortical dysplasia . Magnetic resonance imaging . Myelination . Electroencephalography . Epilepsy . Development Introduction Focal cortical dysplasia (FCD) [1], a form of neuronal migration disorder, is a malformative lesion of the neocortex that occurs during development of the brain. It is widely accepted that FCD can cause intractable epilepsy. Seizures occur at an early age and are often resistant to medication. Surgical resection has been found to be beneficial in these patients [2]. Magnetic resonance imaging (MRI) characteristics of FCD include focal cortical thickening, blurring of the gray– white matter junction, high fluid-attenuated inversion recovery signal, and gyral anatomical abnormalities [3–7]. Not all of the features may be present concurrently; appearances can be subtle and difficult to recognize. One third of patients with histologically confirmed Taylor-type FCD had unremarkable MRI [8, 9]. In this paper, we present a case with negative MRI findings for FCD at the age of 2.5 years that became apparent on repeat MRI at the age of 6 years. Case report
Y. Yamaguchi Department of Pediatrics, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-ku, Fukuoka 812-8582, Japan M. Ohfu Department of Pediatrics, Fukuoka University, 7-45-1 Nanakuma Jonan-ku, Fukuoka 814-0180, Japan
A 6-year-old boy first suffered a generalized tonic seizure at the age of 23 days. Interictal electroencephalogram (EEG) demonstrated a suppression-burst pattern, and he was diagnosed as having early-infantile epileptic encephalopathy with suppression burst (Ohtahara syndrome). EEG still showed a suppression-burst pattern after administration of vitamin B6; however, seizures were almost controlled with zonisamide
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Fig. 1 T1-weighted image (a) and T2-weighted image (b) at the age of 2 years and 6 months demonstrate no abnormalities, although myelination has matured. c Interictal EEG at the age of 1 year reveals frequent spike and spike–wave complexes on the right frontal region (Fp2)
monotherapy. Follow-up EEG was performed at the ages of 1 and 2 years, both of which revealed frequent paroxysmal activity with continuous slow wave on the right frontal region
instead of a suppression-burst pattern (Fig. 1c). MRI at the age of 2 years and 6 months failed to reveal any abnormalities, although myelination was matured (Fig. 1a,b). On follow-up
Fig. 2 T1WI (a) and T2WI (b) at the age of 6 years demonstrates thick cortex and blurring of the gray matter–white matter junction of the right frontal lobe (white arrows). c Ictal EEG at the age of 6 years reveals that almost continuous interictal paroxysmal activity with
maximal amplitude on the right frontal region increase in amplitude (Fp2, underline), followed by generalized attenuation of the background activity (arrow) and reappearance of the ictal activity in the right frontal region (arrowhead) with secondary generalization
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EEG at the age of 3, 4, and 5 years, a high amplitude irregular spike and a spike–slow wave complex were frequently observed over the right frontal area. The patient was admitted to our hospital at the age of 6 years after his seizures became intractable; he had been administered optimal doses of zonisamide and carbamazepine since the age of 5 years and had no neurological deficits other than mental retardation (IQ 44) and hyperkinetic tendency. Long-term video monitoring revealed that his habitual seizure started with the raising of the left hand, soon extending to the right hand, finally developing a generalized convulsion. Seizures occurred once or twice a day. Interictal EEG detected almost continuous paroxysmal activity with maximal amplitude in the right frontal region. Ictal EEG demonstrated increased amplitude of paroxysmal activity in the right frontal region followed by generalized attenuation of background activity and reappearance of ictal activity in the right frontal region with secondary generalization (Fig. 2c). Although interictal positron emission
tomography with 18F-fluorodeoxyglucose showed normal appearances, both the T1-weighted images (T1WI) and T2weighted images on MRI (T2WI) demonstrated a thickened cortex and blurring of the gray–white matter junction of the right frontal lobe (Fig. 2a,b). T2 prolongation of the subcortical white matter was not evident. Right fronto-parietal craniotomy was performed under total intravenous anesthesia with propofol and fentanyl. After opening the dura, the exposed frontal lobe had a normal appearance. Intraoperative electrocorticography (ECoG) revealed frequent localized spikes around the frontal pole (Fig. 3a), visible just above the cortex with blurring of the gray–white matter junction on the intraoperative navigation system (Fig. 3b). This region was slightly elastic on palpation. The anterior parts of the superior and middle frontal gyri were resected using intraoperative ECoG and navigation system guidance. Postoperatively, seizure frequency was markedly decreased, although residual seizures were observed monthly.
Fig. 3 (a) Intraoperative electrocorticogram (nasion reference) over the right frontal lobe demonstrates frequent paroxysmal activity with maximal amplitude of electrode 7 (black arrow), which is located just
above the MRI abnormality on the axial view (b) of the intraoperative navigation system (white arrow)
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Histological findings of the specimen were those of typical FCD (Palmini type IIa), with disorganized cortical lamination and numerous dysmorphic neurons but without balloon cells.
Discussion Blurring of the gray–white matter junction with thickened cortex on T2WI are characteristic MRI findings of FCD [4– 10]. It is suggested that the reduction in the number of myelinated fibers plays an important role in these imaging findings [5]. In the present case, these MRI findings were not evident at the age of 2 years but became apparent at the age of 6 years. Although FCD is congenital condition, the “appearances” of FCD on MRI have been previously demonstrated [5, 11]. Sankar et al. [11] documented three patients aged 4.5–6 months with infantile spasms. Although the first MRI at the age of 6 months showed no abnormalities, the second MRI at the age of 11–36 months revealed T2 hyperintensity in the white matter beneath the dysplastic cortices, with blurring of the gray–white matter junction. Yagishita et al. [5] reported three FCD patients who underwent two or three magnetic resonance (MR) examinations. The first MR studies showed discrimination of the gray–white matter junction in the region of FCD; however, the second or third MR studies clearly demonstrated blurring of the gray–white matter junction and abnormal signal intensity in the white matter. Furthermore, the “disappearance” of FCD findings on serial MRI was also reported. Duprez et al. [12] reported a 2-month-old boy with FCD findings that became indistinguishable on the second MRI at the age of 8 months. Eltze et al. [13] presented four infants with distinct MR appearances of FCD that became subtle on serial MRI. These chronological changes were explained by maturation of myelination, during which the white matter signal on T2WI changes from hyperintense to hypointense and vice versa on T1WI; these MRI changes are completed by the age of 2 years [14]. During maturation, tissue property changes associated with axonal microfilament production, increase in the myelin sheath, and glial cell and glial process multiplication lead to a reduction in free water and resultant shortening of T2 relaxation times. T1 relaxation time shortening, which precedes T2 shortening, is thought to be caused by the interaction of water with cholesterol, galactocerebrocides, and proteins in the myelin membrane [14]. The cortical and subcortical signal appearance associated with FCD can be modified as myelination advances [12]; that the first reported cases with appearance and disappearance of FCD on MRI were performed under the age of 2 years supports this explanation. In the present case, however, the first MRI was performed 2 years after
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completion of myelination, and the signal intensity of the gray and white matter was unchanged on the repeat MRI at the age of 6 years. There was no technical difference between the scans; signal contrast of the gray and white matter is the same on both T1WI and T2WI. Transient T2 signal hyperintensity associated with partial status epilepticus can be ruled out because of the associated T1 signal change. Signal intensity alterations associated with FCD may be explained by an ensemble of histopathological features, including the presence of balloon cells and demyelination of the white matter below the dysplastic cortex [6, 9]. In this case, histological findings were those of Palmini type IIa, with disorganized cortical lamination and numerous dysmorphic neurons but without balloon cells, indicating that balloon cells cannot explain the MRI changes. The exact mechanism of the appearance of FCD findings on MRI after myelination in the present case remains unknown. The region that demonstrated MR changes had been consistently depicted as an area of irritation on EEG. Serial EEG and MRI are both mandatory for follow-up of patients with intractable focal epilepsy.
References 1. Taylor DC, Falconer MA, Bruton CJ, Corsellis JA (1971) Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry 34:369–387 2. Morioka T, Nishio S, Ishibashi H, Muraishi M, Hisada K, Shigeto H, Yamamoto T, Fukui M (1999) Intrinsic epileptogenicity of focal cortical dysplasia as revealed by magnetoencephalography and electrocorticography. Epilepsy Res 33:177–187 3. Bronen RA, Vives KP, Kim JH, Fulbright RK, Spencer SS, Spencer DD (1997) Focal cortical dysplasia of Taylor, balloon cell subtype: MR differentiation from low-grade tumors. Am J Neuroradiol 18:1141–1151 4. Kuzniecky R, Garcia JH, Faught E, Morawetz RB (1991) Cortical dysplasia in temporal lobe epilepsy: magnetic resonance imaging correlations. Ann Neurol 29:293–298 5. Yagishita A, Arai N, Maehara T, Shimizu H, Tokumaru AM, Oda M (1997) Focal cortical dysplasia: appearance on MR images. Radiology 203:553–559 6. Chan S, Chin SS, Nordli DR, Goodman RR, DeLaPaz RL, Pedley TA (1998) Prospective magnetic resonance imaging identification of focal cortical dysplasia, including the non-balloon cell subtype. Ann Neurol 44:749–757 7. Lee BCP, Schmidt RE, Hatfield GA, Bourgeois B, Park TS (1998) MRI of focal cortical dysplasia. Neuroradiology 40:675–683 8. Tassi L, Colombo N, Garbelli R, Francione S, Lo Russo G, Mai R, Cardinale F, Cossu M, Ferrario A, Galli C, Bramerio M, Citterio A, Spreafico R (2002) Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 125:1719–1732 9. Colombo N, Tassi L, Galli C, Citterio A, Lo Russo G, Scialfa G, Spreafico R (2003) Focal cortical dysplasias: MR imaging,
Childs Nerv Syst (2008) 24:269–273 histopathologic, and clinical correlations in surgically treated patients with epilepsy. Am J Neuroradiol 24:724–733 10. Matsuda K, Mihara T, Tottori T, Otubo T, Usui N, Baba K, Matsuyama N, Yagi K (2001) Neuroradiologic findings in focal cortical dysplasia: histologic correlation with surgically resected specimens. Epilepsia 42(Suppl 6):29–36 11. Sankar R, Curran JG, Kevill JW, Rintahaka PJ, Shewmon DA, Vinters HV (1995) Microscopic cortical dysplasia in infantile spasms: evolution of white matter abnormalities. Am J Neuroradiol 16:1265–1272
273 12. Duprez T, Ghariani S, Grandin C, Smith AM, Gadisseux JF, Evrard P (1998) Focal seizure-induced premature myelination: speculation from serial MRI. Neuroradiology 40:580– 582 13. Eltze CM, Chong WK, Bhate S, Harding B, Neville BGR, Cross JH (2005) Taylor-type focal cortical dysplasia in infants: some MRI lesions almost disappear with maturation of myelination. Epilepsia 46:1988–1992 14. Barkovich AJ (2000) Concepts of myelin and myelination in neuroradiology. Am J Neuroradiol 21:1099–1109
