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Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report
Journal of Clinical Neuroscience xxx (2018) xxx–xxx
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Case report
Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report Yasuhiro Takahashi a, Takeshi Mikami a,⇑, Hime Suzuki a, Katsuya Komatsu a, Daisuke Yamamoto b, Shun Shimohama b, Kiyohiro Houkin c, Shintaro Sugita d, Tadashi Hasegawa d, Nobuhiro Mikuni a a
Department of Neurosurgery, Sapporo Medical University, Sapporo, Japan Department of Neurology, Sapporo Medical University, Sapporo, Japan Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo, Japan d Department of Surgical Pathology, Sapporo Medical University, Sapporo, Japan b c
a r t i c l e
i n f o
Article history: Received 6 March 2018 Accepted 22 April 2018 Available online xxxx Keywords: Autoimmune disease LGI1 Limbic encephalitis Quasi-moyamoya disease
a b s t r a c t We report a case of moyamoya disease (MMD), which developed after non-herpetic acute limbic encephalitis (NHALE) associated with anti-leucine-rich glioma-inactivated 1 (LGI1) antibody. The patient’s mother had a history of MMD. No vascular lesions were identified at the time of the NHALE. Nine years later, the patient visited our hospital due to memory disturbances and repeated transient ischemic attacks affecting the right limb. Diffusion-weighted magnetic resonance imaging revealed scattered areas of signal hyperintensity, and the patient was ultimately diagnosed with MMD based on angiography. Revascularization surgery was performed on the left side, where cerebral blood flow was impaired on 123I-N-isopropyl-p-iodoamphetamine single photon emission computed tomography. Postoperatively, the patient was discharged with a normal neurological examination. NHALE associated with LGI1 antibodies is an autoimmune disease. Although autoimmune disease is the most frequent finding other than atherosclerosis in quasi-MMD, this is the first report of NHALE associated with anti-LGI1 antibodies mimicking quasi-MMD. Inflammation and angiogenesis may contribute to the development of MMD, in addition to genetic background. Ó 2018 Elsevier Ltd. All rights reserved.
1. Introduction
2. Case report
Moyamoya disease (MMD) is a cerebrovascular disorder characterized by chronic, progressive, stenotic or occlusive changes in the terminal portions of the bilateral internal carotid arteries (ICAs), which induce an abnormal vascular network composed of collateral pathways at the base of the brain. In cases where MMD occurs in conjunction with various inherited or acquired disease entities [1], the condition has been defined as quasi-MMD. Several reports have noted MMD in association with autoimmune disease [2], though not in association with non-herpetic acute limbic encephalitis (NHALE). Here, we report a case of quasi-MMD, which developed after NHALE with anti-leucine-rich glioma-inactivated 1 (LGI1) antibodies. To our knowledge, this is the first report of NHALE associated with LGI1 antibodies mimicking quasi-MMD.
In 2008, a 41-year-old female was admitted to our hospital due to complaints of headache and memory disturbances. Her mother had a history of MMD. Magnetic resonance imaging (MRI) showed mesial temporal signal hyperintensity on T2-weighted and fluidattenuated inversion recovery (FLAIR) imaging (Fig. 1A, B). The lesion was subsequently excised for the purpose of biopsy. At that time, no vascular abnormalities were identified on magnetic resonance angiography (MRA) and computed tomography angiography (Fig. 1C). The pathological specimen showed lymphocytic infiltration in the perivascular space (Fig. 1D). Postoperatively, convulsive status epilepticus occurred, which was controlled with anticonvulsant medication. Antibody tests were negative for herpes virus and contactin-associated protein-2 (CASPR2), and positive for LGI1 (Fig. 1E). The patient was subsequently diagnosed with NHALE associated with LGI1 antibodies. She was treated with steroid pulse therapy and discharged with a normal neurological examination. However, on follow-up MRI conducted at 3 months, 2 years, 4 years, and 8 years after NHALE, a decreased M1 signal was recognized retrospectively (Fig. 2).
⇑ Corresponding author at: Department of Neurosurgery, Sapporo Medical University, South 1 West 16, Chuo-ku, Sapporo 060-8543, Japan. E-mail address: [email protected] (T. Mikami). https://doi.org/10.1016/j.jocn.2018.04.042 0967-5868/Ó 2018 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
2
Case report / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
Fig. 1. Fluid-attenuated inversion recovery (FLAIR) imaging (A, B) showed signal hyperintensity in the right mesial temporal lobe. No vascular abnormalities were observed on magnetic resonance angiography (MRA) at that time (C). The pathological specimen showed lymphocytic infiltration in the perivascular space (D), and the serum tested positive for anti-leucin-rich glioma-inactivated 1 (anti-LGI1) antibodies (E).
Fig. 2. Follow-up T2-weighted magnetic resonance imaging (MRI) 3 months (A), 2 years (B), 4 years (C), and 8 years (D) after non-herpetic acute limbic encephalitis (NHALE). M1 signal intensity gradually decreased during the follow-up period.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
Case report / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
3
Fig. 3. Diffusion-weighted MRI revealed scattered areas of signal hyperintensity (A), and MRA showed signal reduction of the bilateral internal carotid arteries (ICAs) (B). In the middle cerebral artery (MCA) area, cerebral blood flow on 123I-N-isopropyl-p-iodoamphetamine (123I-IMP) single photon emission computed tomography (SPECT) showed a 17% decrease compared with the right side (C). Cerebral angiography showed bilateral ICA occlusion at the terminal portion and moyamoya vessels (D, F), and collateral flow from the middle meningeal artery. On the left side, collateral circulation had also developed from the craniotomy site (E).
Nine years after the onset of NHALE, the patient returned to our hospital due to memory disturbances and repeated transient ischemic attacks (TIAs) affecting the right limb. Diffusionweighted MRI revealed scattered areas of signal hyperintensity (Fig. 3A). The patient was diagnosed with MMD based on angiography (Fig. 3D–F). The cerebral blood flow value of the left middle cerebral artery (MCA) territory on resting state 123I-N-isopropylp-iodoamphetamine (123I-IMP) single photon emission computed tomography (SPECT) showed a 17% decrease compared with the right side (Fig. 3C). Left superficial temporal artery to MCA bypass was performed. Postoperatively, the TIAs disappeared, and the fullscale IQ (FIQ) score assessed with the Wechsler Adult Intelligence Scale-III (WAIS-III) showed improvement to 88 (from 77 preoperatively). The patient was discharged with a normal neurological examination. 3. Discussion Voltage-gated potassium channel (VGKC) antibodies have been reported in association with neuromyotonia, Morvan’s syndrome, and NHALE. The related autoantibodies are now divided into likely pathogenic entities, which target the extracellular domains of LGI1 and CASPR2 [3]. In quasi-MMD, autoimmune disease is the most frequent underlying disease, except for atherosclerosis. Several reports have noted MMD in association with autoimmune disease, including autoimmune thyroid disease, Type 1 diabetes mellitus, and systemic lupus erythematosus [2]. Chen et al. reported that autoimmune thyroid disease was the first comorbidity associated with MMD [4], and there might be a common pathophysiological mechanism underlying autoimmune thyroid
disease and MMD. Kishitani et al. reported that 21% of their NHALE cases with anti-LGI1 antibodies had anti-NH2-terminal of a-enolase antibodies, which are highly specific for Hashimoto encephalitis, suggesting that NHALE associated with LGI1 antibodies may coincide with Hashimoto disease [5]. In our present case, triiodothyronine (T3) and tetraiodothyronine (T4) levels were low (free T3 [FT3], 2.04; free T4 [FT4], 0.5), though antithyroid microsomal antibody or thyroglobulin antibody were not detected. By contrast, angiogenetic factors, including vascular endothelial growth factor, are thought to play a central role in the signaling cascades in autoimmune diseases associated with quasiMMD [6]. Inflammation and angiogenesis may be involved in the pathogenesis of MMD. Recently, the ring finger protein 213 (RNF213) gene variant p. R4810K was identified as a susceptibility gene for MMD in the East Asian population [7,8]. Although the RNF213 gene p.R4810K variant could not be assessed in the present case, it is found at a high rate in familial cases [7,8]. The p.R4810K variant has also been associated with autoimmune quasi-MMD [9]. Although MMD is not an inflammatory disease, previous data suggest that inflammation might play an important role in MMD development. Namely, the p.R4810K variant plays a unique role in endothelial cells regarding proper gene expression in response to inflammatory signals from the environment [10]. There are few reports concerning de novo development of MMD, and it is difficult to examine the factors associated with the occurrence of MMD. Tashiro et al. reported the clinical course of the de novo development of MMD in an adult female with the p.R4810K variant [11]. It is conceivable that genetic factors might also contribute to the development of quasi-MMD.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
4
Case report / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
References [1] Hayashi K, Horie N, Izumo T, Nagata I. Nationwide survey on quasi-moyamoya disease in Japan. Acta Neurochirur (Wien) 2014;156:935–40. [2] Research Committee on the Pathology and Treatment of. Spontaneous Occlusion of the Circle of Willis. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir 2012;52:245–66. [3] Irani SR, Alexander S, Waters P, Kleopa KA, Pettingill P, Zuliani L, et al. Antibodies to Kv1 potassium channel-complex proteins leucine-rich, glioma inactivated 1 protein and contactin-associated protein-2 in limbic encephalitis, Morvan’s syndrome and acquired neuromyotonia. Brain 2010;133:2734–48. [4] Chen JB, Lei D, He M, Sun H, Liu Y, Zhang H, et al. Clinical features and disease progression in moyamoya disease patients with Graves disease. J Neurosurg 2015;123:848–55. [5] Kishitani T, Matsunaga A, Ikawa M, Hayashi K, Yamamura O, Hamano T, et al. Limbic encephalitis associated with anti-NH2-terminal of a-enolase antibodies: A clinical subtype of Hashimoto encephalopathy. Med (Baltimore) 2017;96:e6181.
[6] Young AM, Karri SK, Ogilvy CS, Zhao N. Is there a role for treating inflammation in moyamoya disease?: a review of histopathology, genetics, and signaling cascades. Front Neurol 2013;4:105. [7] Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PloS One 2011;6:e22542. [8] Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, et al. A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet 2011;56:34–40. [9] Morimoto T, Mineharu Y, Kobayashi H, Harada KH, Funaki T, Takagi Y, et al. Significant association of the RNF213 p. R4810K polymorphism with quasimoyamoya disease. J Stroke Cerebrovasc Dis 2016;25:2632–6. [10] Ohkubo K, Sakai Y, Inoue H, Akamine S, Ishizaki Y, Matsushita Y, et al. Moyamoya disease susceptibility gene RNF213 links inflammatory and angiogenic signals in endothelial cells. Sci Rep 2015;5:13191. [11] Tashiro R, Fujimura M, Niizuma K, Endo H, Sakata H, Sato-Maeda M, et al. De novo development of moyamoya disease in an adult female with a genetic variant of the RNF-213 gene: Case report. J Stroke Cerebrovasc Dis 2017;26: e8–e11.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Case report
Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report Yasuhiro Takahashi a, Takeshi Mikami a,⇑, Hime Suzuki a, Katsuya Komatsu a, Daisuke Yamamoto b, Shun Shimohama b, Kiyohiro Houkin c, Shintaro Sugita d, Tadashi Hasegawa d, Nobuhiro Mikuni a a
Department of Neurosurgery, Sapporo Medical University, Sapporo, Japan Department of Neurology, Sapporo Medical University, Sapporo, Japan Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo, Japan d Department of Surgical Pathology, Sapporo Medical University, Sapporo, Japan b c
a r t i c l e
i n f o
Article history: Received 6 March 2018 Accepted 22 April 2018 Available online xxxx Keywords: Autoimmune disease LGI1 Limbic encephalitis Quasi-moyamoya disease
a b s t r a c t We report a case of moyamoya disease (MMD), which developed after non-herpetic acute limbic encephalitis (NHALE) associated with anti-leucine-rich glioma-inactivated 1 (LGI1) antibody. The patient’s mother had a history of MMD. No vascular lesions were identified at the time of the NHALE. Nine years later, the patient visited our hospital due to memory disturbances and repeated transient ischemic attacks affecting the right limb. Diffusion-weighted magnetic resonance imaging revealed scattered areas of signal hyperintensity, and the patient was ultimately diagnosed with MMD based on angiography. Revascularization surgery was performed on the left side, where cerebral blood flow was impaired on 123I-N-isopropyl-p-iodoamphetamine single photon emission computed tomography. Postoperatively, the patient was discharged with a normal neurological examination. NHALE associated with LGI1 antibodies is an autoimmune disease. Although autoimmune disease is the most frequent finding other than atherosclerosis in quasi-MMD, this is the first report of NHALE associated with anti-LGI1 antibodies mimicking quasi-MMD. Inflammation and angiogenesis may contribute to the development of MMD, in addition to genetic background. Ó 2018 Elsevier Ltd. All rights reserved.
1. Introduction
2. Case report
Moyamoya disease (MMD) is a cerebrovascular disorder characterized by chronic, progressive, stenotic or occlusive changes in the terminal portions of the bilateral internal carotid arteries (ICAs), which induce an abnormal vascular network composed of collateral pathways at the base of the brain. In cases where MMD occurs in conjunction with various inherited or acquired disease entities [1], the condition has been defined as quasi-MMD. Several reports have noted MMD in association with autoimmune disease [2], though not in association with non-herpetic acute limbic encephalitis (NHALE). Here, we report a case of quasi-MMD, which developed after NHALE with anti-leucine-rich glioma-inactivated 1 (LGI1) antibodies. To our knowledge, this is the first report of NHALE associated with LGI1 antibodies mimicking quasi-MMD.
In 2008, a 41-year-old female was admitted to our hospital due to complaints of headache and memory disturbances. Her mother had a history of MMD. Magnetic resonance imaging (MRI) showed mesial temporal signal hyperintensity on T2-weighted and fluidattenuated inversion recovery (FLAIR) imaging (Fig. 1A, B). The lesion was subsequently excised for the purpose of biopsy. At that time, no vascular abnormalities were identified on magnetic resonance angiography (MRA) and computed tomography angiography (Fig. 1C). The pathological specimen showed lymphocytic infiltration in the perivascular space (Fig. 1D). Postoperatively, convulsive status epilepticus occurred, which was controlled with anticonvulsant medication. Antibody tests were negative for herpes virus and contactin-associated protein-2 (CASPR2), and positive for LGI1 (Fig. 1E). The patient was subsequently diagnosed with NHALE associated with LGI1 antibodies. She was treated with steroid pulse therapy and discharged with a normal neurological examination. However, on follow-up MRI conducted at 3 months, 2 years, 4 years, and 8 years after NHALE, a decreased M1 signal was recognized retrospectively (Fig. 2).
⇑ Corresponding author at: Department of Neurosurgery, Sapporo Medical University, South 1 West 16, Chuo-ku, Sapporo 060-8543, Japan. E-mail address: [email protected] (T. Mikami). https://doi.org/10.1016/j.jocn.2018.04.042 0967-5868/Ó 2018 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
2
Case report / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
Fig. 1. Fluid-attenuated inversion recovery (FLAIR) imaging (A, B) showed signal hyperintensity in the right mesial temporal lobe. No vascular abnormalities were observed on magnetic resonance angiography (MRA) at that time (C). The pathological specimen showed lymphocytic infiltration in the perivascular space (D), and the serum tested positive for anti-leucin-rich glioma-inactivated 1 (anti-LGI1) antibodies (E).
Fig. 2. Follow-up T2-weighted magnetic resonance imaging (MRI) 3 months (A), 2 years (B), 4 years (C), and 8 years (D) after non-herpetic acute limbic encephalitis (NHALE). M1 signal intensity gradually decreased during the follow-up period.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
Case report / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
3
Fig. 3. Diffusion-weighted MRI revealed scattered areas of signal hyperintensity (A), and MRA showed signal reduction of the bilateral internal carotid arteries (ICAs) (B). In the middle cerebral artery (MCA) area, cerebral blood flow on 123I-N-isopropyl-p-iodoamphetamine (123I-IMP) single photon emission computed tomography (SPECT) showed a 17% decrease compared with the right side (C). Cerebral angiography showed bilateral ICA occlusion at the terminal portion and moyamoya vessels (D, F), and collateral flow from the middle meningeal artery. On the left side, collateral circulation had also developed from the craniotomy site (E).
Nine years after the onset of NHALE, the patient returned to our hospital due to memory disturbances and repeated transient ischemic attacks (TIAs) affecting the right limb. Diffusionweighted MRI revealed scattered areas of signal hyperintensity (Fig. 3A). The patient was diagnosed with MMD based on angiography (Fig. 3D–F). The cerebral blood flow value of the left middle cerebral artery (MCA) territory on resting state 123I-N-isopropylp-iodoamphetamine (123I-IMP) single photon emission computed tomography (SPECT) showed a 17% decrease compared with the right side (Fig. 3C). Left superficial temporal artery to MCA bypass was performed. Postoperatively, the TIAs disappeared, and the fullscale IQ (FIQ) score assessed with the Wechsler Adult Intelligence Scale-III (WAIS-III) showed improvement to 88 (from 77 preoperatively). The patient was discharged with a normal neurological examination. 3. Discussion Voltage-gated potassium channel (VGKC) antibodies have been reported in association with neuromyotonia, Morvan’s syndrome, and NHALE. The related autoantibodies are now divided into likely pathogenic entities, which target the extracellular domains of LGI1 and CASPR2 [3]. In quasi-MMD, autoimmune disease is the most frequent underlying disease, except for atherosclerosis. Several reports have noted MMD in association with autoimmune disease, including autoimmune thyroid disease, Type 1 diabetes mellitus, and systemic lupus erythematosus [2]. Chen et al. reported that autoimmune thyroid disease was the first comorbidity associated with MMD [4], and there might be a common pathophysiological mechanism underlying autoimmune thyroid
disease and MMD. Kishitani et al. reported that 21% of their NHALE cases with anti-LGI1 antibodies had anti-NH2-terminal of a-enolase antibodies, which are highly specific for Hashimoto encephalitis, suggesting that NHALE associated with LGI1 antibodies may coincide with Hashimoto disease [5]. In our present case, triiodothyronine (T3) and tetraiodothyronine (T4) levels were low (free T3 [FT3], 2.04; free T4 [FT4], 0.5), though antithyroid microsomal antibody or thyroglobulin antibody were not detected. By contrast, angiogenetic factors, including vascular endothelial growth factor, are thought to play a central role in the signaling cascades in autoimmune diseases associated with quasiMMD [6]. Inflammation and angiogenesis may be involved in the pathogenesis of MMD. Recently, the ring finger protein 213 (RNF213) gene variant p. R4810K was identified as a susceptibility gene for MMD in the East Asian population [7,8]. Although the RNF213 gene p.R4810K variant could not be assessed in the present case, it is found at a high rate in familial cases [7,8]. The p.R4810K variant has also been associated with autoimmune quasi-MMD [9]. Although MMD is not an inflammatory disease, previous data suggest that inflammation might play an important role in MMD development. Namely, the p.R4810K variant plays a unique role in endothelial cells regarding proper gene expression in response to inflammatory signals from the environment [10]. There are few reports concerning de novo development of MMD, and it is difficult to examine the factors associated with the occurrence of MMD. Tashiro et al. reported the clinical course of the de novo development of MMD in an adult female with the p.R4810K variant [11]. It is conceivable that genetic factors might also contribute to the development of quasi-MMD.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042
4
Case report / Journal of Clinical Neuroscience xxx (2018) xxx–xxx
References [1] Hayashi K, Horie N, Izumo T, Nagata I. Nationwide survey on quasi-moyamoya disease in Japan. Acta Neurochirur (Wien) 2014;156:935–40. [2] Research Committee on the Pathology and Treatment of. Spontaneous Occlusion of the Circle of Willis. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir 2012;52:245–66. [3] Irani SR, Alexander S, Waters P, Kleopa KA, Pettingill P, Zuliani L, et al. Antibodies to Kv1 potassium channel-complex proteins leucine-rich, glioma inactivated 1 protein and contactin-associated protein-2 in limbic encephalitis, Morvan’s syndrome and acquired neuromyotonia. Brain 2010;133:2734–48. [4] Chen JB, Lei D, He M, Sun H, Liu Y, Zhang H, et al. Clinical features and disease progression in moyamoya disease patients with Graves disease. J Neurosurg 2015;123:848–55. [5] Kishitani T, Matsunaga A, Ikawa M, Hayashi K, Yamamura O, Hamano T, et al. Limbic encephalitis associated with anti-NH2-terminal of a-enolase antibodies: A clinical subtype of Hashimoto encephalopathy. Med (Baltimore) 2017;96:e6181.
[6] Young AM, Karri SK, Ogilvy CS, Zhao N. Is there a role for treating inflammation in moyamoya disease?: a review of histopathology, genetics, and signaling cascades. Front Neurol 2013;4:105. [7] Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PloS One 2011;6:e22542. [8] Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, et al. A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet 2011;56:34–40. [9] Morimoto T, Mineharu Y, Kobayashi H, Harada KH, Funaki T, Takagi Y, et al. Significant association of the RNF213 p. R4810K polymorphism with quasimoyamoya disease. J Stroke Cerebrovasc Dis 2016;25:2632–6. [10] Ohkubo K, Sakai Y, Inoue H, Akamine S, Ishizaki Y, Matsushita Y, et al. Moyamoya disease susceptibility gene RNF213 links inflammatory and angiogenic signals in endothelial cells. Sci Rep 2015;5:13191. [11] Tashiro R, Fujimura M, Niizuma K, Endo H, Sakata H, Sato-Maeda M, et al. De novo development of moyamoya disease in an adult female with a genetic variant of the RNF-213 gene: Case report. J Stroke Cerebrovasc Dis 2017;26: e8–e11.
Please cite this article in press as: Takahashi Y et al. Development of moyamoya disease after non-herpetic acute limbic encephalitis: A case report. J Clin Neurosci (2018), https://doi.org/10.1016/j.jocn.2018.04.042