Manual and automated tissue segmentation confirm the impact of thalamus atrophy on cognition in multiple sclerosis: A multicenter study,NeuroImage: Clinical

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Manual and automated tissue segmentation confirm the impact of thalamus atrophy on cognition in multiple sclerosis: A multicenter study
NeuroImage: Clinical ( IF 3.4 ) Pub Date : 2020-12-25 , DOI: 10.1016/j.nicl.2020.102549
Jessica Burggraaff ₁ , Yao Liu ₂ , Juan C Prieto ₃ , Jorge Simoes ₁ , Alexandra de Sitter ₂ , Serena Ruggieri ₄ , Iman Brouwer ₂ , Birgit I Lissenberg-Witte ₅ , Mara A Rocca ₆ , Paola Valsasina ₇ , Stefan Ropele ₈ , Claudio Gasperini ₉ , Antonio Gallo ₁₀ , Deborah Pareto ₁₁ , Jaume Sastre-Garriga ₁₂ , Christian Enzinger ₁₃ , Massimo Filippi ₁₄ , Nicola De Stefano ₁₅ , Olga Ciccarelli ₁₆ , Hanneke E Hulst ₁₇ , Mike P Wattjes ₁₈ , Frederik Barkhof ₁₉ , Bernard M J Uitdehaag ₁ , Hugo Vrenken ₂ , Charles R G Guttmann ₃ ,

Affiliation

Department of Neurology, MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, Location VUmc, De Boelelaan 1117, 1118, 1081 HV Amsterdam, The Netherlands.
Department of Radiology and Nuclear Medicine, MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, Location VUmc, De Boelelaan 1117, 1118, 1081 HV Amsterdam, The Netherlands.
Center for Neurological Imaging, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, 1249 Boylston Street, Boston, MA 02215, USA.
Department of Human Neurosciences, "Sapienza" University of Rome, Piazzale Aldo Moro, 5, 00185 Roma RM, Italy; Department of Neurosciences, San Camillo Forlanini Hospital, Circonvallazione Gianicolense, 87, 00152 Roma RM, Italy.
Department of Epidemiology and Biostatistics, Amsterdam UMC, Location VUmc, De Boelelaan 1089a, 1081 HV Amsterdam, the Netherlands.
Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, and Neurology Unit, San Raffaele Scientific Institute, Via Olgettina, 58, 20132 Milano MI, Italy; Neurology Unit, San Raffaele Scientific Institute, Via Olgettina, 58, 20132 Milano MI, Italy.
Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, and Neurology Unit, San Raffaele Scientific Institute, Via Olgettina, 58, 20132 Milano MI, Italy.
Department of Neurology, Medical University of Graz, Auenbruggerplatz 22, 8036 Graz, Austria.
Department of Neurosciences, San Camillo Forlanini Hospital, Circonvallazione Gianicolense, 87, 00152 Roma RM, Italy.
Division of Neurology and 3T MRI Research Center, Department of Advanced Medical and Surgical Sciences, University of Campania "Luigi Vanvitelli", Viale Abramo Lincoln, 5, 81100 Caserta, CE, Napoli, Italy.
Section of Neuroradiology and MRI Unit, Department of Radiology, University Hospital iValld'Hebron, Autonomous University of Barcelona, Passeig de la Vall d'Hebron 119-129, 08035 Barcelona, Spain.
Department of Neurology, University Hospital iValld'Hebron, Autonomous University of Barcelona, Passeig de la Vall d'Hebron 119-129, 08035 Barcelona, Spain.
Division of Neuroradiology, Vascular and Interventional Radiology, Department of Radiology, Medical University of Graz, Auenbruggerplatz 22, 8036 Graz, Austria.
Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, and Neurology Unit, San Raffaele Scientific Institute, Via Olgettina, 58, 20132 Milano MI, Italy; Neurology Unit, San Raffaele Scientific Institute, Via Olgettina, 58, 20132 Milano MI, Italy; Neurophysiology Unit, San Raffaele Scientific Institute, and (14)Vita-Salute San Raffaele University, Via Olgettina, 58, 20132 Milano, MI, Italy; Department of Neurological and Behavioural Sciences, University of Siena, 53100 Siena SI, Italy.
Department of Neurological and Behavioural Sciences, University of Siena, 53100 Siena SI, Italy.
Department of Neuroinflammation UCL, Queen Square Institute of Neurology UCL, Queen Square, London WC1N 3BG, United Kingdom.
Department of Anatomy and Neurosciences, Amsterdam Neuroscience, MS Center Amsterdam, Amsterdam UMC, Vrije Universiteit Amsterdam, De Boelelaan 1108, P.O. Box 7057, 1007 MB, Amsterdam, The Netherlands.
Department of Radiology and Nuclear Medicine, MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, Location VUmc, De Boelelaan 1117, 1118, 1081 HV Amsterdam, The Netherlands; Department of Diagnostic and Interventional Neuroradiology, Hannover Medical School, Hannover, Carl-Neuberg-Straße, 30625 Hannover, Germany.
Department of Radiology and Nuclear Medicine, MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, Location VUmc, De Boelelaan 1117, 1118, 1081 HV Amsterdam, The Netherlands; Institutes of Neurology & Healthcare Engineering, UCL, 235 Euston Rd, Bloomsbury, London NW1 2BU, United Kingdom.

Background and rationale

Thalamus atrophy has been linked to cognitive decline in multiple sclerosis (MS) using various segmentation methods. We investigated the consistency of the association between thalamus volume and cognition in MS for two common automated segmentation approaches, as well as fully manual outlining.

Methods

Standardized neuropsychological assessment and 3-Tesla 3D-T1-weighted brain MRI were collected (multi-center) from 57 MS patients and 17 healthy controls. Thalamus segmentations were generated manually and using five automated methods. Agreement between the algorithms and manual outlines was assessed with Bland-Altman plots; linear regression assessed the presence of proportional bias. The effect of segmentation method on the separation of cognitively impaired (CI) and preserved (CP) patients was investigated through Generalized Estimating Equations; associations with cognitive measures were investigated using linear mixed models, for each method and vendor.

Results

In smaller thalami, automated methods systematically overestimated volumes compared to manual segmentations [ρ=(-0.42)-(-0.76); p-values < 0.001). All methods significantly distinguished CI from CP MS patients, except manual outlines of the left thalamus (p = 0.23). Poorer global neuropsychological test performance was significantly associated with smaller thalamus volumes bilaterally using all methods. Vendor significantly affected the findings.

Conclusion

Automated and manual thalamus segmentation consistently demonstrated an association between thalamus atrophy and cognitive impairment in MS. However, a proportional bias in smaller thalami and choice of MRI acquisition system might impact the effect size of these findings.

中文翻译：

手动和自动组织分割证实丘脑萎缩对多发性硬化症认知的影响：一项多中心研究

背景和基本原理

丘脑萎缩已通过多种分割方法与多发性硬化症（MS）的认知能力下降相关。我们调查了两种常用的自动分割方法以及完全手动概述的丘脑体积与MS认知之间关联的一致性。

方法

从57名MS患者和17名健康对照者中（多中心）收集了标准化的神经心理学评估和3-Tesla 3D-T1加权脑MRI。丘脑分割是手动生成的，并使用五种自动化方法生成。算法的算法和手册轮廓之间的一致性是通过Bland-Altman图进行评估的。线性回归评估了比例偏差的存在。通过广义估计方程研究了分割方法对认知障碍（CI）和保留（CP）患者分离的影响。对于每种方法和供应商，使用线性混合模型调查与认知测度的关联。

结果

在较小的海水中，与手动分割相比，自动化方法会系统地高估体积[ ρ =（-0.42）-（-0.76）; p-值<0.001）。除左丘脑的手动轮廓外，所有方法均将CI与CP MS患者区分开来（p = 0.23）。使用所有方法，较差的整体神经心理测试性能与双侧较小的丘脑体积显着相关。供应商严重影响了调查结果。