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Default Mode Network Connectivity Is Associated with Long-Term Clinical NeuroImage: Clinical 22 (2019) 101805 Contents lists available at ScienceDirect NeuroImage: Clinical journal homepage: www.elsevier.com/locate/ynicl Default mode network connectivity is associated with long-term clinical outcome in patients with schizophrenia T ⁎ Hyeongrae Leea, Dong-Kyun Leea, Kyeongwoo Parka, Chul-Eung Kimb, Seunghyong Ryua, a Department of Mental Health Research, National Center for Mental Health, Seoul, Republic of Korea b Mental Health Research Institute, National Center for Mental Health, Seoul, Republic of Korea ARTICLE INFO ABSTRACT Keywords: This study investigated whether resting-state functional connectivity is associated with long-term clinical out- Schizophrenia comes of patients with schizophrenia. Resting-state brain images were obtained from 79 outpatients with Outcome schizophrenia and 30 healthy controls (HC), using a 3 T-MRI scanner. All patients were 20–50 years old Functional connectivity with > 3 years' duration of illness and appeared clinically stable. We assessed their psychopathology using the Default mode network 18-item Brief Psychiatric Rating Scale (BPRS-18) and divided them into “good,”“moderate,” and “poor” out- Resting-state come (SZ-GO, SZ-MO, and SZ-PO) groups depending on BPRS-18 total score. We obtained individual functional connectivity maps between a seed region of the bilateral posterior cingulate cortex (PCC) and all other brain regions and compared the functional connectivity of the default mode network (DMN) among the HC and 3 schizophrenia outcome groups, with a voxel-wise threshold of P < .001 within a cluster-extent threshold of 114 voxels. Additionally, we assessed correlations between functional connectivity and BPRS-18 scores. The SZ-MO and SZ-PO groups showed decreased functional connectivity between PCC and right ventromedial prefrontal cortex (vmPFC), left middle cingulate cortex, and left frontopolar cortex (FPC) compared to the SZ-GO and HC groups. DMN connectivity in the right vmPFC and left FPC negatively correlated with subscale scores of the BPRS-18, except the negative symptoms subscale. In this study, poorer clinical outcomes in patients with schizophrenia were associated with decreased DMN connectivity. In particular, the decreased functional con- nectivity might be related to the severity of positive and mood symptoms rather than negative symptoms. 1. Introduction have moderate to severe symptoms and functional impairments (Menezes et al., 2006). Schizophrenia is a mental illness characterized by delusions, hal- Neuroimaging markers associated with the clinical course and out- lucinations, disordered formal thought, disorganized behaviors, nega- come of schizophrenia have been studied. Structural magnetic re- tive symptoms, and cognitive dysfunctions (Kahn et al., 2015). The sonance imaging (sMRI) studies have shown that patients with poor outcomes of schizophrenia vary widely among individuals, but the outcomes have more marked reductions in total and regional gray majority of patients with schizophrenia experience residual symptoms matter volume, and greater ventricular enlargement, compared to those and impaired social functioning. The positive symptoms, such as de- with good outcomes (Kubota et al., 2015; Wojtalik et al., 2017). lusions and hallucinations, tend to relapse and remit, although some Functional MRI (fMRI) studies have reported widespread network patients suffer from treatment-resistant residual psychotic symptoms dysconnectivity in schizophrenia (Yu et al., 2012), but the relationship (Bertelsen et al., 2009). Even after patients achieve remission from between dysconnectivity and long-term clinical course of schizophrenia psychotic symptoms, the negative symptoms and cognitive dysfunctions remains unknown. Considering evidence of progressive loss of synaptic tend to be chronic, which leads to impairments in social and occupa- activity in patients with schizophrenia (Marsman et al., 2013), clinical tional functioning (Buchanan, 2007). In terms of course and outcome of progression or deterioration in schizophrenia might be associated with schizophrenia, it is generally known that approximately one-third of impaired control of synaptic plasticity leading to dysfunctional in- patients have a relatively good outcome, with no more than mild tegration of neural systems, i.e., dysconnectivity (Friston, 1999; Friston symptoms and functional impairments, and the remaining two-thirds and Frith, 1995; Stephan et al., 2006). ⁎ Corresponding author at: Department of Mental Health Research, National Center for Mental Health, 127 Youngmasan-ro, Gwangjin-gu, Seoul 04933, Republic of Korea. E-mail address: [email protected] (S. Ryu). https://doi.org/10.1016/j.nicl.2019.101805 Received 14 December 2018; Received in revised form 17 March 2019; Accepted 30 March 2019 Available online 01 April 2019 2213-1582/ © 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). H. Lee, et al. NeuroImage: Clinical 22 (2019) 101805 Table 1 Demographic and clinical characteristics of study participants. Variablesa Healthy controls (N = 30) Outcome groups of patients with schizophrenia Statisticsb Good (N = 25) Moderate (N = 31) Poor (N = 23) Age, y 37.60 ± 7.02 41.00 ± 7.07 37.77 ± 7.51 37.26 ± 6.97 F = 1.50, P = .220 Sex (male / female), n 15 (50.0) / 15 (50.0) 15 (60.0) / 10 (40.0) 16 (51.6) / 15 (48.4) 12 (52.2) / 11 (47.8) χ2 = 0.63, P = .890 Education, y 14.77 ± 3.15 13.00 ± 3.25 12.68 ± 1.66 12.61 ± 2.17 F = 4.32, P = .007 Duration of illness, y – 16.56 ± 7.01 16.42 ± 8.17 16.61 ± 8.00 F < 0.01, P = 1.00 Antipsychotic dose (chlorpromazine equivalent), mg – 626.81 ± 394.17 860.83 ± 464.93 1035.43 ± 605.26 F = 4.22, P = .018 BPRS-18 total score – 26.60 ± 2.92 36.52 ± 2.80 46.70 ± 3.47 F = 260.98, P < .001 Affect subscale – 5.48 ± 1.19 7.58 ± 2.54 8.78 ± 2.88 F = 12.59 P < .001 Positive symptoms subscale – 6.00 ± 1.87 9.71 ± 2.34 12.83 ± 2.08 F = 62.12 P < .001 Negative symptoms subscale – 7.24 ± 2.13 9.00 ± 2.31 12.09 ± 2.13 F = 29.65 P < .001 Resistance subscale – 3.32 ± 0.56 5.00 ± 1.53 6.83 ± 2.57 F = 25.12 P < .001 Activation subscale – 3.56 ± 1.04 4.23 ± 1.02 5.17 ± 1.07 F = 14.41 P < .001 WHODAS 2.0 total score – 13.17 ± 5.29 17.87 ± 6.51 28.14 ± 6.82 F = 35.84, P < .001 Abbreviations: BPRS-18, 18-item Brief Psychiatric Rating Scale; WHODAS 2.0, WHO Disability Assessment Schedule 2.0. a Mean ± SD or N(%). b ANOVA or chi-square test. fMRI studies have demonstrated aberrant functioning of the default by no exacerbation of psychotic symptoms and no change in general mode network (DMN) in schizophrenia. The DMN, a distributed net- clinical state and medication for at least 3 months prior to the time of work composed of a set of brain regions including the medial prefrontal assessment. We excluded patients with a concurrent axis I diagnosis cortex (mPFC), posterior cingulate cortex (PCC), precuneus, and lat- according to the DSM-IV, current or past neurological disease, any eral/medial temporal lobes (Fox and Raichle, 2007; Fransson, 2005), contraindication to MRI scan, or a physical condition that would render shows increased activation during rest or internal cognitive processing, an MRI scan difficult to administer or interpret, e.g., severe extra- but decreased activation during externally goal-directed cognitive tasks pyramidal symptoms. The HCs consisted of volunteers from the local (Raichle et al., 2001). DMN alterations have also been associated with community who were free of any history of psychiatric disorders. The various symptoms of schizophrenia, including positive, negative, and same exclusion criteria that were applied to the patients also applied to disorganized symptoms (Camchong et al., 2011; Rotarska-Jagiela et al., the HC group with regard to medical, neurological, and physical con- 2010; Whitfield-Gabrieli et al., 2009). In addition, recent studies have ditions. Data from 79 patients and 30 HCs were included in the final reported reduced DMN suppression during a broad range of cognitive analysis. tasks in patients with schizophrenia, which could be interpreted as the This study was initiated after approval of the Institutional Review cause or the consequence of cognitive deficits (Fornito et al., 2012; Board of the National Center for Mental Health (IRB approval number: Pomarol-Clotet et al., 2008). Considering that persistent, unremitting 116271–2017-26), and written informed consent was obtained from all psychotic symptoms, prominent negative symptoms, and more severe subjects. cognitive impairments are clinical factors that suggest poor prognosis (Lang et al., 2013), DMN abnormalities may be associated with the course and outcome of individuals with schizophrenia. 2.2. Clinical assessments and group assignment This study investigated the relationship between DMN connectivity and long-term clinical outcomes of schizophrenia. Accordingly, we We defined long-term outcome of schizophrenia as overall severity performed PCC seed region connectivity analysis using resting-state of residual psychopathology in clinically stable patients with chronic functional MRI data and compared DMN connectivity among healthy schizophrenia whose clinical progression was considered to have controls (HCs) and 3 groups of patients with chronic schizophrenia who reached a plateau after 3 years of onset. The overall level of the patient's were considered to have good, moderate, and poor outcomes (SZ-GO, psychopathology was evaluated by a psychiatrist (S.R.), who used the SZ-MO, and SZ-PO). In addition, we examined correlations between 18-item Brief Psychiatric Rating Scale (BPRS-18) (Overall and Gorham, DMN connectivity and psychopathology in patients with schizophrenia. 1962). Leucht et al. (2005) proposed that “mildly ill” according to the Clinical Global Impression (CGI) scale corresponds to BPRS-18 total scores of 18–31 and “moderately ill” corresponds to BPRS-18 total 2. Materials and methods scores of 32–41. Based on these criteria, we classified the patients into 3 groups: SZ-GO (BPRS-18 total scores of 18–31, N = 25), SZ-MO (BPRS- 2.1.
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