Association of Visual Impairment in Neuromyelitis Optica Spectrum Disorder With Visual Network Reorganization

Finke, Carsten; Zimmermann, Hanna; Pache, Florence; Oertel, Frederike Cosima; Chavarro, Velina S.; Kramarenko, Yelyzaveta; Bellmann‐Strobl, Judith; Ruprecht, Klemens; Brandt, Alexander U.; Paul, Friedemann

doi:10.1001/jamaneurol.2017.3890

Cited by 40 publications

(27 citation statements)

References 52 publications

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“…The optic radiation (OR) is an integral part of the afferent visual system and belongs to the most frequently affected white matter pathways in autoimmune neuroinflammatory disorders of the central nervous system, i.e. multiple sclerosis (MS) and neuromyelitis optica spectrum disorders (NMOSD) ( Backner et al, 2018 ; Balcer et al, 2015 ; Bennett et al, 2015 ; Finke et al, 2018 ; Martínez-Lapiscina et al, 2014 ; Pache et al, 2016a , Pache et al, 2016b ; Pache et al, 2016a , Pache et al, 2016b ; Petzold et al, 2014 ; Pfueller and Paul, 2011 ; Scheel et al, 2014 ; Schmidt et al, 2017 ; Sinnecker et al, 2015b ; Wingerchuk et al, 2015 ). Diffusion-weighted magnetic resonance imaging (DW-MRI) yields the potential to non-invasively investigate microstructural OR integrity ( Assaf and Pasternak, 2008 ; Filippi et al, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Comparison of probabilistic tractography and tract-based spatial statistics for assessing optic radiation damage in patients with autoimmune inflammatory disorders of the central nervous system

Kuchling

Backner

Oertel

et al. 2018

NeuroImage: Clinical

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BackgroundDiffusion Tensor Imaging (DTI) can evaluate microstructural tissue damage in the optic radiation (OR) of patients with clinically isolated syndrome (CIS), early relapsing-remitting multiple sclerosis and neuromyelitis optica spectrum disorders (NMOSD). Different post-processing techniques, e.g. tract-based spatial statistics (TBSS) and probabilistic tractography, exist to quantify this damage.ObjectiveTo evaluate the capacity of TBSS-based atlas region-of-interest (ROI) combination with 1) posterior thalamic radiation ROIs from the Johns Hopkins University atlas (JHU-TBSS), 2) Juelich Probabilistic ROIs (JUEL-TBSS) and tractography methods using 3) ConTrack (CON-PROB) and 4) constrained spherical deconvolution tractography (CSD-PROB) to detect OR damage in patients with a) NMOSD with prior ON (NMOSD-ON), b) CIS and early RRMS patients with ON (CIS/RRMS-ON) and c) CIS and early RRMS patients without prior ON (CIS/RRMS-NON) against healthy controls (HCs).MethodsTwenty-three NMOSD-ON, 18 CIS/RRMS-ON, 21 CIS/RRMS-NON, and 26 HCs underwent 3 T MRI. DTI data analysis was carried out using JUEL-TBSS, JHU-TBSS, CON-PROB and CSD-PROB. Optical coherence tomography (OCT) and visual acuity testing was performed in the majority of patients and HCs.ResultsAbsolute OR fractional anisotropy (FA) values differed between all methods but showed good correlation and agreement in Bland-Altman analysis. OR FA values between NMOSD and HC differed throughout the methodologies (p-values ranging from p < 0.0001 to 0.0043). ROC-analysis and effect size estimation revealed higher AUCs and R2 for CSD-PROB (AUC = 0.812; R2 = 0.282) and JHU-TBSS (AUC = 0.756; R2 = 0.262), compared to CON-PROB (AUC = 0.742; R2 = 0.179) and JUEL-TBSS (AUC = 0.719; R2 = 0.161). Differences between CIS/RRMS-NON and HC were only observable in CSD-PROB (AUC = 0.796; R2 = 0.094). No significant differences between CIS/RRMS-ON and HC were detected by any of the methods.ConclusionsAll DTI post-processing techniques facilitated the detection of OR damage in patient groups with severe microstructural OR degradation. The comparison of distinct disease groups by use of different methods may lead to different - either false-positive or false-negative - results. Since different DTI post-processing approaches seem to provide complementary information on OR damage, application of distinct methods may depend on the relevant research question.

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Section: Introductionmentioning

confidence: 99%

Comparison of probabilistic tractography and tract-based spatial statistics for assessing optic radiation damage in patients with autoimmune inflammatory disorders of the central nervous system

Kuchling

Backner

Oertel

et al. 2018

NeuroImage: Clinical

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“…43,45 A study focusing on the visual system of patients with NMOSD and previous ON has shown increase in the functional connectivity of the primary visual network compared with those without ON. 11 These findings were also associated with greater retinal damage and reduced visual acuity, suggesting an attempt at cortical reorganization. Similar findings were seen in our previous work, showing an increase in visual network connectivity in patients with CIS-ON compared with CIS-nON.…”

Section: Discussionmentioning

confidence: 98%

“…Moreover, our previous works have emphasized the importance of activity along the visual dorsal stream in patients with ON, 6-10 but our works on connectivity have used wholenetwork resolution. 10,11 Therefore, to examine whether there are specific connectivity changes within the visual network, we herein used graph theory methods, 12,13 focusing on its regional measures to pinpoint which visual regions are more affected.…”

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confidence: 99%

Cortical topological network changes following optic neuritis

Backner

Ben-Shalom

Kuchling

et al. 2020

Neurol Neuroimmunol Neuroinflamm

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ObjectiveTo differentiate between visual cortical network topology changes following optic neuritis (ON) stemming from different inflammatory disease types, we used mathematical graph theory-based tools to analyze functional imaging data. MethodsSixty-two patients were recruited into this cross-sectional study, 23 of whom had neuromyelitis optica spectrum disorder (NMOSD) with ON, 18 with clinically isolated syndrome (CIS)-ON, and 21 with other CIS episodes. Twenty-six healthy controls (HCs) were also recruited. All participants underwent resting-state functional MRI. Visual networks were defined using 50 visual regions of interest. Analysis included graph theory metrics, including degree, density, modularity, and local and global efficiency. ResultsVisual network density shows decreased connectivity in all patient groups compared with controls. A higher degree of connections is seen in both ON groups (CIS and NMOSD) compared with the the non-ON group. This pattern is most pronounced in dorsal-lateral regions. Information transfer efficiency and modularity were reduced in both CIS groups, but not in the NMOSD group, compared with the HC group. ConclusionsVisual network density appears affected by the neurologic deficit sustained (ON), and connectivity changes are more evident in dorsal-lateral regions. Efficiency and modularity appear to be associated with the specific disease type (CIS vs NMOSD). Thus, topological cortical changes in the visual system are associated with the type of neurologic deficit within the limits set on them by the underlying pathophysiology. We suggest that cortical patterns of activity should be considered in the outcome of the patients despite the localized nature of ON. Complex network analysis is based on graph theory, a mathematical approach to networks. Briefly, the method requires definition of brain regions as nodes and the search for connections, or edges, between those nodes. These connections, anatomic or functional, can then be thresholded and binarized into connectivity matrices, representing the existence or lack of connection between any 2 nodes in the network. From these matrices, various measures can be extracted to quantify network topology and organization (figure 1).Glossary CIS = clinically isolated syndrome; EDSS = Expanded Disability Status Scale; FEF = frontal eye field; FLAIR = fluid-attenuated inversion recovery; HC = healthy control; NMOSD = neuromyelitis optica spectrum disorder; nON = nonoptic neuritis; ON = optic neuritis; ROI = region of interest; RS-fMRI = resting-state functional MRI.

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“…Using fMRI, Rocca et al (2004) showed an irregular form of movement associated with cortical activation in patients with NMOSD that extended beyond the sensorimotor network and involved the visual network of the brain. Previous studies (Lopes et al, 2015;Cai et al, 2017) have also explored visual cortex FC in NMOSD but did not give an account on its association with the clinical data such as their disease duration or frequency of optic neuritis attack; two previous reports (Lopes et al, 2015;Finke et al, 2018) used the activation fMRI approach and showed increased connectivity in NMOSD patients when compared to healthy controls. Cai et al (2017) used the seed-based approach, similar to our current approach, and showed decreased connectivity in the higher visual cortex.…”

Section: Discussionmentioning

confidence: 99%

“…The mean time series from all of the voxels within the ROI was used as the seed reference time series, and the Pearson's correlation coefficient (between the average time series for that seed and each voxel in the brain) was computed as the strength of FC. For further statistical analysis, the correlation coefficients were transformed to z-values using the Fisher r-to-z transformation to improve the normality of the correlation coefficients (Finke et al, 2018). Thus, a map that represented the FC strength and the seed region (in terms of the z-values for each subject) was obtained.…”

Section: Mri Data Preprocessingmentioning

confidence: 99%

Alterations in the Brain Structure and Functional Connectivity in Aquaporin-4 Antibody-Positive Neuromyelitis Optica Spectrum Disorder

et al. 2020

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Purpose: To investigate the mechanisms underlying the gray matter volume (GMV) and functional connectivity (FC) changes in aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder (NMOSD) patients. Methods:This cross-sectional study consisted of 21 patients with aquaporin-4 antibody-positive NMOSD and 22 age-and sex-matched healthy controls. All participants underwent cerebral magnetic resonance imaging and testing each individual's visual acuity was done.Results: Neuromyelitis optica spectrum disorder patients showed significantly reduced GMV in the left calcarine, left thalamus and right lingual gyrus of the NMOSD patients when compared to HC (P < 0.05). NMOSD patients showed significantly decreased FC values (P < 0.05) in both the left and right calcarine, right lingual gyrus and left thalamus, respectively, when compared to HC. We also observed a positive correlation between the FC values of the left thalamus, bilateral calcarine gyrus and the visual acuity, respectively (P < 0.05). Furthermore, a negative association was seen between the duration of the disease, frequency of optic neuritis, and the FC values in the lingual gyrus, bilateral calcarine gyrus, and right lingual gyrus, respectively (P < 0.05). Conclusion:Reduced visual acuity and frequency of optic neuritis are associated with alterations in the GMV and FC in NMOSD. Our current study, which provides imaging evidence on the impairment involved in NMOSD, sheds light on pathophysiological responses of optic neuritis attack on the brain especially on the visual network.

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Association of Visual Impairment in Neuromyelitis Optica Spectrum Disorder With Visual Network Reorganization

Cited by 40 publications

References 52 publications

Comparison of probabilistic tractography and tract-based spatial statistics for assessing optic radiation damage in patients with autoimmune inflammatory disorders of the central nervous system

Comparison of probabilistic tractography and tract-based spatial statistics for assessing optic radiation damage in patients with autoimmune inflammatory disorders of the central nervous system

Cortical topological network changes following optic neuritis

Alterations in the Brain Structure and Functional Connectivity in Aquaporin-4 Antibody-Positive Neuromyelitis Optica Spectrum Disorder

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