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Network Centrality in Patients with Acute Unilateral Open Globe Injury: a Voxel‑Wise Degree Centrality Study

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Network Centrality in Patients with Acute Unilateral Open Globe Injury: a Voxel‑Wise Degree Centrality Study MOLECULAR MEDICINE REPORTS 16: 8295-8300, 2017 Network centrality in patients with acute unilateral open globe injury: A voxel‑wise degree centrality study HUA WANG1, TING CHEN1, LEI YE2, QI-CHEN YANG3, RONG WEI2, YING ZHANG2, NAN JIANG2 and YI SHAO1,2 1Department of Ophthalmology, Xiangya Hospital, Central South University, Changsha, Hunan 410008; 2Department of Ophthalmology, The First Affiliated Hospital of Nanchang University, Jiangxi Province Clinical Ophthalmology Institute and Oculopathy Research Centre, Nanchang, Jiangxi 330006; 3Eye Institute of Xiamen University, Fujian Provincial Key Laboratory of Ophthalmology and Visual Science, Xiamen, Fujian 361102, P.R. China Received January 12, 2017; Accepted August 1, 2017 DOI: 10.3892/mmr.2017.7635 Abstract. The present study aimed to investigate functional Introduction networks underlying brain-activity alterations in patients with acute unilateral open globe injury (OGI) and associations with Open globe injury (OGI) is a severe eye disease that frequently their clinical features using the voxel-wise degree centrality causes unilateral visual loss. Ocular trauma is a public health (DC) method. In total, 18 patients with acute OGI (16 males and problem in developing countries (1,2). A previous study indicated 2 females), and 18 healthy subjects (16 males and 2 females), that the annual prevalence of ocular trauma was 4.9 per 100,000 closely matched in age, sex and education, participated in the in the Western Sicily Mediterranean area, which investigated a present study. Each subject underwent a resting-state functional 5 year period from January 2001 to December 2005 (3). In addi- magnetic resonance imaging scan. The DC method was used tion, the incidence of OGI is increased in men compared with to assess local features of spontaneous brain activity. Receiver women (4). OGI primarily occurs in the 15-44 and 0-14 age operating characteristic curve analysis was used to distinguish groups (5). A total of ~19 million cases of unilateral blindness OGIs from healthy controls (HCs). Correlation analysis was or decreased vision are caused by ocular trauma each year (6). used to examine the association between the observed mean Clinically, OGI is frequently associated with corneal injury DC values of different brain areas and behavioral perfor- and iris prolapse (7), retinal detachment (8), glaucoma (9) and mance. Compared with HCs, patients with acute unilateral endophthalmitis (10). At present, surgery is the principal means OGI had significantly increased DC values in the bilateral of treatment for OGI (11,12). primary visual cortex (V1/V2) and left precuneus (PCUN), Computed tomography (CT) and B-scan ultrasonography and significantly decreased DC values in the right insula, left are important clinical tests for the diagnosis of OGI. Although insula, right inferior parietal lobule (IPL)/supramarginal gyrus CT may provide information for the diagnosis of OGI (13), (SMG), IPL/SMG, right supplementary motor area and right it is insufficient for making the decision of immediate treat- postcentral gyrus. Additionally, in the acute OGI group, it was ment (14). B-scan ultrasonography is able to locate retinal observed that the duration of OGI was negatively correlated detachment points, retinal tears and vitreous traction, and with the DC signal value of the bilateral V1/V2 (r=-0.581; thus may be beneficial for further medical treatment (15). P=0.011) and left PCUN (r=-0.508; P=0.031). Acute OGI led The aforementioned methods focus solely on ocular trauma to brain functional network dysfunction in a number of brain in OGI. However, other parts of the visual system, including regions, which may indicate impairment of the visual cortex the connecting pathways and the visual cortex, are frequently and other vision-associated brain regions in OGI. overlooked. Little is known about the underlying mechanisms of neural alterations in the OGI. Resting-state functional magnetic resonance imaging (fMRI) is able to evaluate intrinsic brain activity in subjects at rest (16). It has been widely used in visual studies associated Correspondence to: Dr Yi Shao, Department of Ophthalmology, with brain functional alterations. A previous study reported The First Affiliated Hospital of Nanchang University, Jiangxi Province Clinical Ophthalmology Institute and Oculopathy Research Centre, decreased functional connectivity within the occipital visual 17 Yong Wai Zheng Street, Dong Hu, Nanchang, Jiangxi 330006, cortices and a correlation with other vision-associated brain P. R. Ch i na regions in patients with early blindness (17). An additional E-mail: [email protected] study demonstrated that patients with early blindness exhib- ited stronger connectivity in the primary somatosensory area Key words: open globe injury, functional magnetic resonance (S1) and primary visual cortex (V1) compared with patients imaging, voxel-wise degree centrality, resting state with late blindness (18). In addition, a previous report demon- strated that patients with early blindness exhibited markedly decreased gray matter volumes in the optic tract and visual 8296 WANG et al: NETWORK CENTRALITY STUDY IN PATIENTS WITH OGI cortex (19). Although there have been numerous studies into MRI data acquisition. MRI scanning was performed on a visual and brain function alterations in patients with blind- 3-Tesla MR scanner (Trio; Siemens AG, Munich, Germany). ness, less is known about the spontaneous brain activity High-resolution T1-weighted images were acquired as alterations in patients with acute unilateral vision loss caused described previously (30). A total of 240 functional images by OGI. covering the whole brain in one subject were obtained. Voxel-wise degree centrality (DC) is a measurement that illustrates the network architecture of functional connectivity fMRI data preprocessing. All functional data were prefil- within the human brain connectome at the voxel level (20). tered using MRIcro (www.MRIcro.com) and preprocessed Distinct from the amplitude of low-frequency fluctuation using SPM8 (www.fil.ion.ucl.ac.uk/spm), DPARSFA (ALFF) (21) and regional homogeneity (ReHo) (22) tech- (rfmri.org/DPARSF) and the Resting-state Data Analysis niques, it does not require the definition of regions of interest. Toolkit (www.restfmri.net), as described previously (30). The DC method is able to provide insights into the functional connectivity of the entire brain. The DC method has been Degree centrality. The voxel-wise functional network was successfully used to evaluate the pathological mechanisms generated as described previously (30). Based on the voxel-wise underlying a number of diseases, including autism (23), functional network, DC was calculated as the counting of obesity (24) and Parkinson's disease (25). A previous study significant suprathresholded correlations (or the degree of the investigated strabismus and optic neuritis through whole-brain binarized adjacency matrix) for each subject. The voxel-wise voxel-based analysis of diffusion tensor imaging (26,27). In DC map for each individual was converted into a z-score map, addition, ALFF and ReHo were previously used to analyzed as described previously (30). patients with acute OGI (28,29). The present study evaluated functional network brain activity alterations in patients with Statistical analysis. For demographic and clinical measure- acute unilateral vision loss caused by OGI, and associations ments, the data were presented as the mean ± standard deviation. with clinical features. The differences in clinical features between the patients and HCs were calculated using independent two-sample t-tests. Subjects and methods Independent t-tests with generalized linear model analysis was performed using the SPM8 toolkit to investigate the group Subjects. A total of 18 patients with acute unilateral OGI differences in DC values between patients with OGI and HCs. (16 male and 2 female; 8 right eye injury and 8 left eye injury; P<0.05 was considered to indicate a statistically significant age range, 18-65 years) were recruited from the ophthalmology difference, with Gaussian random field theory correction. departments of the First Affiliated Hospital of Nanchang Pearson correlation analysis was used to calculate the associa- University and Xiangya Hospital between August 2015 and tion between mean DC values and clinical features. Statistical January 2016. Acute unilateral OGI was diagnosed with the tests were performed using SPSS version 16.0 (SPSS, Inc., following critera: i) Severe ocular trauma; ii) acute vision loss; Chicago, IL, USA). iii) corneal and scleral rupture; iv) decreased intraocular pres- sure; v) incomplete eyeball wall visualized using orbital CT Results or orbital MRI; and vi) contralateral eye best-corrected visual acuity (VA) ≥1.0. Demographics and visual measurements. There were no Exclusion conditions were as follows: i) Patients with other significant differences in weight (P=0.423), age (P=0.990), eye diseases (including cataracts, glaucoma, pterygium and best-corrected VA-right (P<0.001) and best-corrected VA-left strabismus, ocular infection and inflammation, hereditary (P<0.001) between the two groups (Table I). optic neuropathy, ischemic diseases, demyelinating diseases, intraocular placeholder lesions, toxic lesions, vascular lesions DC differences. Compared with HCs, DC values of patients and ischemic optic neuropathy); ii) central nervous system with acute OGI were increased in the bilateral visual cortex diseases and systemic disorders; iii)
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