Dynamic change in magnetic resonance imaging of patients with neuromyelitis optica.

Just Accepted by International Journal of Neuroscience

Dynamic change in magnetic resonance imaging of patients with neuromyelitis optica Yongxiang Fan, Fulan Shan, Shao-Peng Lin, Youming long, Bin Liang, Cong Gao, Qingchun Gao doi:10.3109/00207454.2015.1055356

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Abstract Objective: To analyze changes in magnetic resonance imaging (MRI) of spinal cord lesions in neuromyelitis optica (NMO) and the correlation between segmental length of spinal cord lesions and Expanded Disability Status Scale (EDSS) scores. Methods: Twenty-five patients with confirmed NMO were examined from the Second Affiliated Hospital of Guangzhou Medical University, China. The information collected included their treatment, MRI, laboratory tests, and EDSS scores at different stages. Results: All cases exhibited spinal cord lesions, with 23 (92%) having longitudinally extensive transverse myelitis (extending ≥ 3 vertebral segments). There was positive correlation between segmental length of spinal cord lesions and EDSS scores: during the acute phase, r D 0.430 (P D 0.032); during remission, r D 0.605 (P D 0.002). Enlarged spinal cord lesions and swelling were found in eighteen cases (72%) during the acute phase, and four cases (16%, P D 0.000) after 6 months of treatment. Lesion enhancement was found in seventeen cases (68%) during the acute phase, and eight cases (32%, P D 0.023) 6 months of treatment. Leptomeningeal enhancement was found in three cases during the acute phase, which disappeared after treatment. Atrophy of spinal cord lesions occurred in two cases. Changes in lesions were statistically significant (P D 0.006) 12 months of treatment. Conclusion: Positive correlation was found between segmental length of spinal cord lesions and EDSS scores, which was more significant during remission. After 6 months of regular treatment, restorative changes compared with the acute phase were found by MRI.

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Publisher: Informa Healthcare Journal: International Journal of Neuroscience DOI: http://dx.doi.org/10.3109/00207454.2015.1055356

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Dynamic change in magnetic resonance imaging of patients with neuromyelitis

Yongxiang Fan1,2, Fulan Shan1,2, Shao-Peng Lin1,3, Youming long1,2, Bin

1

Key Laboratory of Neurogenetics and Channelopathies of Guangdong Province and

cSe pTt eAd CM Can Eu

The Ministry of Education of China, Institute of Neuroscience and the Second

Affiliated Hospital of GuangZhou Medical University, 250# Changgang east Road, GuangZhou, 510260, Guangdong Province, China. 2

Department of Neurology, the Second Affiliated Hospital of GuangZhou Medical

University, 250# Changgang east Road, GuangZhou, 510260 Guangdong Province, China. 3

Department of Emergency, the Second Affiliated Hospital of Guangzhou Medical

University, 250# Changgang East Road, Guangzhou 510260, Guangdong province, China.

Yongxiang Fan and Fulan Shan are the first authors.

Correspondence author at: Key Laboratory of Neurogenetics and Channelopathies of

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Liang1,2,Cong Gao1,2*, Qingchun Gao1,2

Guangdong Province and The Ministry of Education of China, Institute of Neuroscience and The Second Affiliated Hospital of GuangZhou Medical University, 250# Changgang east Road, GuangZhou, 510260 Guangdong Province, China. Tel: +86-020-3415-3147; Fax: +86-020-3415-3147 Email: [email protected].


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Objective: To analyze changes in magnetic resonance imaging (MRI) of spinal cord lesions in neuromyelitis optica (NMO) and the correlation between segmental length of spinal cord lesions and Expanded Disability Status Scale (EDSS) scores. Methods: Twenty-five patients with confirmed NMO were examined from the Second Affiliated Hospital of Guangzhou Medical University, China. The information collected included their treatment, MRI, laboratory tests, and EDSS scores at different stages. Results: All cases exhibited spinal cord lesions, with 23 (92 %) having longitudinally extensive transverse myelitis (extending ≥ 3 vertebral segments). There was positive correlation between segmental length of spinal cord lesions and EDSS scores: during the acute phase, r = 0.430 (P = 0.032); during remission, r = 0.605 (P = 0.002). Enlarged spinal cord lesions and swelling were found in eighteen cases (72 %) during the acute phase, and four cases (16 %, P = 0.000) after 6 months of treatment. Lesion enhancement was found in seventeen cases (68 %) during the acute phase, and eight cases (32 %, P = 0.023) 6 months of treatment. Leptomeningeal enhancement was found in three cases during the acute phase, which disappeared after treatment. Atrophy of spinal cord lesions occurred in two cases. Changes in lesions were statistically significant (P = 0.006) 12 months of treatment. Conclusion: Positive correlation was found between segmental length of spinal cord lesions and EDSS scores, which was more significant during remission. After 6 months of regular treatment, restorative changes compared with the acute phase were found by MRI.

Key words: NMO; MRI; EDSS;Dynamic Change;

Running title: Changes of MRI in NMO Word count: 2090

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Abstract

Introduction Neuromyelitis optica (NMO) is an immune-mediated inflammatory demyelinating


At present, the general diagnostic criteria for NMO follows the Wingerchuk 2006 criteria [1]: necessary conditions: optic neuritis and acute myelitis; with two or more of the following criteria: 1. contiguous spinal cord magnetic resonance imaging (MRI) lesion extending over three vertebral segments; 2. brain MRI not meeting diagnostic criteria for multiple sclerosis (MS); 3. NMO-immunoglobulin G (IgG) seropositivity. MRI has an incomparable advantage in the diagnosis of NMO and is important in monitoring disease progression and condition [2]. In previous studies, most analyses of NMO imaging focused on MRI characteristics during the acute phase or in comparison with MS. In this study, we dynamically analyzed the MRI characteristics of NMO, including changes in spinal cord lesions, and analyzed the correlation between segmental length of spinal cord lesions and Expanded Disability Status Scale (EDSS) scores. Patients and methods

1.1 Inclusion and exclusion criteria Inclusion criteria: Patients admitted to the Second Affiliated Hospital of Guangzhou Medical University, China, from January 2007 to August 2013, who met the diagnostic criteria of Wingerchuk 2006 [1], and had follow-up periods greater than 12 months, with complete clinical and radiographic data. The diagnostic criteria of Optic neuritis: Acute vision loss, with or without eye sore and papillary edema; Vision abnormalities; Relative afferent papillary defect, Visual Evoked Potential(VEP) anomalies [3]. Exclusion criteria: follow-up periods less than 12 months; lack of complete clinical and imaging data; negativity for aquaporin 4 (AQP4) antibody detection, or symptoms hard to distinguish from infection or cancer. 1.2 Research methods

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cord.

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disease of the central nervous system, mainly involving the optic nerves and spinal

All patients suspected of NMO were examined for AQP4 expression using an

AQP4 antibody and cell-based assay [4]. All of their clinical and imaging data, including general information, clinical manifestation, laboratory tests and imaging results, were collected. Among them, 25 patients were diagnosed with NMO, according to the Wingerchuk 2006 criteria, and had complete clinical and imaging data.

Their courses of disease were divided into four phases: the acute stage, 3 months, 6 months, and 12 months after onset. Subsequently, we recorded their MRI characteristics, especially the number of segmental spinal cord lesions of the four

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Results


2.1 General information (Table 1) Patients were aged between 18–58 years old (mean 41.7 ± 12.3). Twenty-two cases were female (88 %), and three were male (12 %). Only one case (4 %) relapsed within 12 months, while eleven cases (44 %) relapsed during the follow-up period. 2.2 Treatment options Acute phase: high-dose (500 mg/day for 5–7 days) intravenous methylprednisolone and immunoglobulin. Remission: methylprednisolone (40 mg/day), with 11 patients also receiving azathioprine. The dosages of methylprednisolone were reduced gradually when the disease stabilized. 2.3 Lesion distribution during the acute phase of NMO All 25 patients had spinal cord lesions: 23 patients had longitudinally extensive transverse myelitis (LETM) lesions; nine (36 %) cases were cervical; four (16 %) cases were thoracic; five (20 %) cases had both cervical and thoracic lesions; while another five (20 %) cases had thoracic and lumbar myeloid lesions. In the remaining two patients, one had lesions located in the oblongata dorsal (Figure 1), while the other had central tube expansion and brain lesion in the peri-ependymal areas and the diencephalon by MRI. 2.4 Correlation between segmental length of spinal cord lesions and EDSS scores There was a positive correlation between the number of segmental spinal cord lesions and EDSS scores: the correlation coefficient was 0.430 (P = 0.032) during the acute phase; while it was 0.605 (P = 0.002) during the remission phase (Figure 2). The initial length of spinal cord lesion is not correlated to final EDSS (P=0.187), and there is no correlation between initial EDSS and the final EDSS (P=0.243).

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different phases. EDSS scores were also graded for all patients. The median time of all follow-ups was 32 months (13–84 months). 1.3 Statistical analysis Statistical analysis was conducted using the Statistical Program for Social Sciences version 13.0 (SPSS13.0). Spearman correlation analysis was performed to examine the correlation between segmental length of spinal cord lesions and EDSS scores; Chi-square or Fisher's exact tests were used for binary and categorical data. One-way analysis of variance (ANOVA) was used for continuous variables. Nonparametric tests were used for data without normal distribution. A value of P < 0.05 was considered statistically significant.

EDSS scores after treatment were statistically significantly different compared with

the acute phase (P < 0.0001). The segmental length of the spinal cord lesions reduced after 3 months compared with the acute phase (P = 0.267); the length of the lesions further reduced after 6 months of treatment (P = 0.052); and noticeably reduced after 12 months of treatment (P = 0.006).

2.5 Dynamic changes of spinal cord lesions in NMO In the acute phase, more than three edematous lesions extended along the spinal cord. Eighteen (72 %) cases had swelling lesions during the acute phase, eleven (44 %)

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cases after 3 months of treatment (P = 0.085), and four (16 %) cases after 6 months of

treatment (P < 0.0001). Following treatment, the LETM lesions began to fragment into multiple smaller lesions, before almost disappearing (Figure 3).

acute phase (Figure 4).

Lesion enhancement occurred in seventeen (68 %) cases during the acute phase,


twelve (48 %) cases after 3 months (P = 0.252), and eight (32 %) cases after 6 months (P = 0.023). In this study, we found three cases had leptomeningeal enhancement in

the spinal cord during the acute phase. This phenomenon disappeared after 6 months of treatment (Figure 5).

In this study, we also found that atrophy occurred in lesions of the spinal cord in

two cases, and the atrophy progressed with time (Figure 6).

Only one case (4 %) relapsed during the 12 months post disease-onset. Eleven cases

(44 %) relapsed during the 1-year follow-up after onset.

In this cohort study, eight cases had brain abnormalities. Brain lesions showed spots

or patched abnormalities. The lesions were located in the brainstem, hypothalamus, adjacent to lateral ventricles, and deep white matter. The cranial lesions reduced after treatment (Figure 7). Discussion

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Furthermore, five (20 %) cases had no obvious swelling of the lesion during the

NMO is an autoimmune disorder of the central nervous system, predominately

affecting the optic nerves and the spinal cord. The onset of NMO can happen at any age, with the median age being 35–45 years. There is a higher prevalence of NMO in women than men [5, 6]. In our study, the median age was 44 years, and the average age was 41.7 ± 12.3 years, with a higher ratio of women to men (7:1). MRI has indispensable importance in the diagnosis and management of NMO. Our MRI data showed that 23 cases had LETM, with lesions greater than three vertebral

segments, consistent with the diagnostic criteria for NMO. In a previous study, seropositive NMO was shown to have significantly longer lesions than those in our study, spanning a mean of 4.5–8.7 spinal cord segments [7]. According to the EDSS,

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patients with a scoring from 1.0 to 4.5 have normal walking function, whereas a scoring from 4.5 to 9.5 indicates walking dysfunction. There was a positive correlation between

the number of segmental spinal cord lesions and EDSS scores, with higher EDSS scores corresponding to longer spinal cord lesions. The correlation appeared to be more

LETM is a MRI characteristic of NMO [8]. In this study, 23 cases (92 %) had obvious LETM lesions, consistent with previous studies of spinal cord lesion


characteristics [9,10]. With treatment, LETM lesions can shrink and appear fragmented [11]. During the follow-up, we found that the length of segmental spinal cord lesions were shorter after treatment. This size reduction was statistically more significant at 12 months compared with 6 months.

During the acute phase, the spinal cord lesions were swollen and enhanced,

indicating active lesions [12]. Spinal cord lesions are hypersensitive on T2-weighted MRI scans. The spinal lesions often involve the cervical and thoracic segments, located in the central spinal cord [13]. During the chronic phase of NMO, the lesions of spinal cords appear thinner, some even exhibiting atrophy [14]. In the 25 cases of this study, 17 cases had enhancement of lesions, while 18 cases exhibited swelling of lesions. After treatment, both of these abnormal phenomena disappeared. In particular, after 6 months of treatment, the change in these abnormalities was significantly different.

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significant during the remission phase.

Furthermore, two cases exhibited atrophy in lesion-area of the spinal cords subsequently. This phenomenon was consistent with previous study[14], in which there was atrophy of spinal cord lesions in the advanced stages of disease. Brain lesions are a common occurrence in NMO [15,16,17,18]. In this study, there were eight (32 %) cases with brain lesions, consistent with previous studies [19]. Brain lesions of NMO localize at sites of high AQP4 expression, such as the hypothalamus,

periventricular areas, the third or fourth ventricle, the lateral ventricles and brainstem [20,21]. In our study, we found brain lesions located in the brainstem, hypothalamus,

adjacent to the lateral ventricles, and in deep white matter. In a previous report, almost all of the NMO patients with contrast-enhanced lesions had a cloud-like enhancement pattern [22,23]. In our study, three patients had leptomeningeal enhancement in the

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spinal cord during the acute phase. To date, this phenomenon is still relatively unreported. Furthermore, whether the enhancement of this phenomenon is related to patient clinical manifestations needs further study.

Another finding of our study was the detection of a small brain lesion localized in

was localized in the mesencephalon cerebral peduncle. Another patient also had a

lesion localized near the thalamus. After treatment, the lesion near the thalamus


disappeared and a new lesion near the lateral ventricles appeared. This phenomenon is similar to the change of lesions that occur with MS [20], which should be further investigated.

In this study, one case (4 %) relapsed at 12 months after onset. The spinal cord lesions of this patient disappeared after 6 months of regular treatment, following which she discontinued treatment after medical advice. After 2 months, she experienced weakness, numbness and had difficulty urinating. MRI revealed obvious lesions similar to the lesions of the first onset. The other 24 patients adhered to their regular treatment and had no relapse during their follow-up, indicating that it is very important to inform patients of adherence to regular therapy, which include hormone and azathioprine maintenance therapy for the prevention of disease recurrence [24]. In summary, MRI is a useful tool in the diagnosis and assessment of NMO. There is a positive correlation between the segmental length of spinal cord lesion and EDSS scores, which was more significant during remission. Lesion swelling and enhancement can disappear with time. After 6 months of regular treatment, restorative changes compared with the acute phase were found by MRI.

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the medulla oblongata during the acute phase. After 6 months of treatment, this lesion

Conflict of interest statement

The authors have declared that no competing interests exist.

Funding/Support This research work was supported by the Science and Technology plan project of Guangdong Province (2012B031800240), the National Science Foundation of China (NSFC) (No. 81100890).

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relapses in neuromyelitis optica: a retrospective analysis. Mult Scler,2007,13: 968-974.

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weakness after blurred vision fifteen days previous, also suffering from a cold and fever seven days earlier. Seropositive for aquaporin 4. T2-weighted magnetic resonance imaging showed no lesion present in thoracic spinal cord during the acute stage (A), 3 months after treatment (B), 6 months after treatment (C), 1 year after treatment (D), with corresponding EDSS at each stage of 8.5, 4.5, 3.0, and 2.5, respectively.

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Figure 1. Sixteen-year-old female, presented with progressive right facial and left limb

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and 1 year. During the acute phase, the expanded disability status scale (EDSS) scores

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Figure 2. Linear graphs obtained during the acute phase and at 3 months, 6 months,

were higher because the length of the spinal cord lesions were increased. (A) Changes in EDSS after treatment over time. (B) Changes in lesions after treatment over time. (C) Correlation between EDSS and lesions during acute phase; (D) Correlation between EDSS and lesions during chronic phase.

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showed dynamic changes of the spinal cord lesion. (A) Obvious swelling of the lesion during the acute phase. (B) The swollen lesion area reduced after 3 months of treatment. (C) The swollen lesion mostly disappeared after 6 months of treatment. (D) The lesion recurred 1 year after onset. Corresponding EDSS at each stage were 8.0, 4.5, 3.0, and 1.5, respectively.

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Figure3. Forty-seven-year old female; contrast magnetic resonance imaging

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27-year old female, who presented with blurred vision and limb weakness after exposure to rain, was seropositive for aquaporin 4. Acute phase (A1, A2); 3 months after treatment (B); 6 months after treatment (C); 1 year after disease onset (D). Corresponding EDSS at each stage were 8.5, 4.5, 3.0, and 1.0, respectively.

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Figure 4. Contrast magnetic resonance images of the cervical spinal cord from a

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cSe pTt eAd CM Can Eu disappeared progressively with time after treatment (B, C, D).

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Figure5. Leptomeningeal enhancement presented during the acute stage (A), which

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hyperintense signal during the acute stage on T2-weighted MRI; (B) the swollen lesion reduced with blurring of the hyperintense signal at 3 months after onset; (C) the spinal cord showed moderate atrophy at 6 months after onset; (D) the spinal cord showed severe atrophy at 12 months after onset. Corresponding EDSS at each stage were 8.5, 4.5, 3.5, 3.5, respectively.

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Figure 6. The lesion in spinal cord changed over time: (A) swollen lesion with

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