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Gray Matter Volume Changes Following Antipsychotic Therapy in First Journal of Psychiatric Research 116 (2019) 126–132 Contents lists available at ScienceDirect Journal of Psychiatric Research journal homepage: www.elsevier.com/locate/jpsychires Gray matter volume changes following antipsychotic therapy in first-episode schizophrenia patients: A longitudinal voxel-based morphometric study T Fan Guoa,b,1, Yuan-Qiang Zhua,1, Chen Lia,1, Xing-Rui Wanga, Hua-Ning Wangd, Wen-Ming Liud, ∗ ∗∗ Liu-Xian Wanga,c, Ping Tiana, Xiao-Wei Kanga, Long-Biao Cuia,e, Yi-Bin Xia, , Hong Yina, a Department of Radiology, Xijing Hospital, Fourth Military Medical University, Xi'an, 710032, China b Key Laboratory of Molecular Imaging of the Chinese Academy of Sciences, Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, China c Department of Radiology, Chinese PLA General Hospital, Beijing, China d Department of Psychiatry, Xijing Hospital, Fourth Military Medical University, Xi'an, 710032, China e Department of Clinical Psychology, School of Medical Psychology, Fourth Military Medical University, Xi'an, 710032, China ARTICLE INFO ABSTRACT Keywords: Despite evidence of structural brain abnormalities in schizophrenia, the current study aimed to explore the Schizophrenia effects of antipsychotic treatment on gray matter (GM) volume using structural magnetic resonance imaging Voxel-based morphometry (MRI) and investigate the relationship between brain structure and treatment response. The GM volumes of 33 Antipsychotics patients with first-episode schizophrenia were calculated with voxel-based morphometry (VBM), with 33 mat- Magnetic resonance imaging ched healthy controls. Longitudinal volume changes within subjects after 4-month antipsychotic treatment were First-episode also evaluated. Correlation between volumetric changes and clinical symptoms derived from the Positive and Gray matter volume Negative Syndrome Scale (PANSS) were further investigated. Compared with healthy controls, decreased GM volumes in the frontal gyrus were observed in schizophrenia patients. After 4-month treatment, patients showed significantly decreased GM volume primarily in the bilateral frontal, temporal and left parietal brain regions. In addition, the GM volume changes of the left postcentral gyrus was positively correlated with negative symptoms improvement, and the correlation analysis revealed the total PANSS scores changes were associated with GM volume changes in the right inferior frontal gyrus and the right superior temporal gyrus. Besides, non-responders had reduced GM volume in the bilateral middle frontal gyrus and the right superior frontal gyrus compared with responders and healthy controls. Our results suggest that the abnormality in the right frontal gyrus exists in the early stage of schizophrenia. Moreover, the relationship between antipsychotics and structural changes was identified. The GM volume might have the potential to reflect the symptom improvement in schizophrenia patients. And MRI may assist in predicting the antipsychotic treatment response in first-episode schizophrenia patients. 1. Introduction understanding the pathophysiology of schizophrenia, especially in the early stage of the disease. Schizophrenia is a complex psychotic disorder characterized by Progressive reductions in brain volume have been reported in long- abnormal behavior, confused thinking and auditory verbal hallucina- term studies after onset of first psychotic symptoms (Haijma et al., tion. The presence of gray matter (GM) volume abnormalities in schi- 2013; Olabi et al., 2011). It was assumed that besides the disease pro- zophrenia patients, primarily the reductions in the frontal and temporal gression, antipsychotic treatment could at least in part be related to the cortex, insula, etc, have been reported in numerous imaging studies GM loss (Emsley et al., 2017; Fusar-Poli et al., 2013). Thus longitudinal (Honea et al., 2005; Shepherd et al., 2012; Wright et al., 2000). How- design study is crucial to evaluate the treatment effect for schizophrenia ever, some studies reported increased GM volume or no structural dif- patients. A few studies investigating structural brain abnormalities in ferences in schizophrenic patients (Bruder et al., 1999; Knochel et al., first-episode schizophrenia patients have reported inconsistent results. 2016). Therefore, studying first-episode patient is helpful for For example, Yue et al. reported increased GM volume in the bilateral ∗ Corresponding author. No. 127 Changle West Road, Xi'an, Shaanxi, 710032, China. ∗∗ Corresponding author. No. 127 Changle West Road, Xi'an, Shaanxi, 710032, China. E-mail addresses: [email protected] (Y.-B. Xi), [email protected] (H. Yin). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.jpsychires.2019.06.009 Received 20 December 2018; Received in revised form 13 June 2019; Accepted 14 June 2019 0022-3956/ © 2019 Elsevier Ltd. All rights reserved. F. Guo, et al. Journal of Psychiatric Research 116 (2019) 126–132 prefrontal cortex, insula, thalamus and left superior occipital cortex generation antipsychotic drugs, including risperidone, olanzapine, pa- (Yue et al., 2016). A meta-analysis reported a reduction of GM volume liperidone, amisulpride and aripiprazole. For the present study, treat- after antipsychotic treatments (Fusar-Poli et al., 2013). Moreover, ment response was operationally defined using criteria described pre- previous studies have mostly focused on the long-term progression in viously (Andreasen et al., 2005). In brief, specific items from PANSS GM changes at least for years (Emsley et al., 2017; Ho et al., 2011; were chosen including the positive symptoms of delusions (P1), con- Veijola et al., 2014). Short term study is still lacking for understanding ceptual disorganization (P2) and hallucinatory behavior (P3), the ne- whether the progressive changes in GM was related to antipsychotic gative symptoms of blunted affect (N1), social withdrawal (N4) and treatment. lack of spontaneity (N6), the general psychopathology of mannerisms/ The controversial results from those longitudinal studies might be posturing (G5) and unusual thought content (G9). And any of the above explained as follows: First, typical and atypical antipsychotics could mentioned item with a score > 3 was considered as non-response. lead to different pharmacological actions and thus induce brain struc- Based on the response criteria, 22 patients were classified as responders tures changes differently (Dazzan et al., 2005; Yue et al., 2016). Second, and 11 patients were classified as non-responders. the dose of antipsychotics, the observation intervals and symptom se- verity could all affect the nature of the pathophysiologic process of 2.3. Image acquisition schizophrenia thus make the progressive brain changes a matter of speculation (Haijma et al., 2013; Ho et al., 2011; Vita et al., 2015; Brain imaging data were acquired with a 3.0-Teslaa GE MRI scanner Zhang et al., 2018). Moreover, how the patients react to the anti- equipped with an eight-channel receiver head coil. Contiguous axial psychotics is also worth discussing. Therefore, considering the above images using a 3D Bravo T1-weighted sequence across the entire brain mentioned factors, especially the patients’ responses to antipsychotics, were acquired with the following parameters: repetition time = 8.2 ms, could help us better identify the important brain structures during the echo time = 3.2 ms, flip angle = 12°, matrix size = 256 × 256, slice treatment. thickness = 1 mm, field of view = 256 × 256 mm2, and voxel To enhance our understanding of structural brain alterations in size = 1 × 1 × 1 mm3. patients with schizophrenia, the current study was to investigate the effects of illness and antipsychotic treatment on morphologic changes 2.4. Image processing and analysis in first-episode schizophrenia patients using whole-brain voxel-based morphometry (VBM). We first investigated whole brain structural All of the T1-weighed MRI images were processed using the voxel- changes by comparing first-episode schizophrenia with healthy con- based morphometry (VBM) toolbox in the FMRIB Software Library trols. The influence of atypical antipsychotics on changes in GM volume (FSL), as one reliable measurement for evaluating GM volume (Schnack after 16 weeks of atypical antipsychotic treatment were further ex- et al., 2010; Xing and Zuo, 2018). In Detail, structural data was pro- amined. Finally, we hypothesized that VBM factors could predict cessed with FSL 5.0.10 software. First, brain extracting tool (BET) was treatment response. We aimed to ascertain which structural brain employed to cut the skull from all T1 MRI structural images (Smith, changes would reflect the clinical moderators including antipsychotics 2010); Next, FSL Automated Segmentation Tool (FAST) was adopted to responses and illness severity. carry out tissue-type segmentation (Zhang et al., 2001); the segmented GM parietal volume images were then aligned to the MNI standard 2. Material and methods space (MNI152) by applying linear image registration tool FLIRT and nonlinear registration FNIRT methods. A study-specific template was 2.1. Subjects created by averaging the registered images, to which the native GM images were then non-linearly re-registered. The registered GM parietal Thirty-three subjects diagnosed with first-episode schizophrenia volume images were modulated for the contraction/enlargement due to were recruited from the Department of Psychiatry for the present study. the nonlinear component of the transformation by dividing them by the All
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