David Romero-Bascones

Mondragon University

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Maitane Barrenechea

Mondragon University

Unai Ayala

Mondragon University

Iñigo Gabilondo

BioCruces Health research Institute

Axel Petzold

University College London

Pearse A. Keane

National Institute for Health Research

Juan Carlos Gómez‐Esteban

University of the Basque Country

Ane Murueta‐Goyena

University of the Basque Country

Siegfried Wagner

University College London

Sara Teijeira‐Portas

BioCruces Health research Institute

Jugnoo S. Rahi

University College London

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University College London

UK Biobank

Moorfields Eye Hospital NHS Foundation Trust

Moorfields Eye Hospital

National Institute for Health Research

Institute of Ophthalmology

Queen's University Belfast

National Health Service

University of Oxford

McGill University

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Foveal Remodeling of Retinal Microvasculature in Parkinson’s Disease

Frontiers in Neuroscience (2021)

Ane Murueta‐Goyena Maitane Barrenechea Asier Erramuzpe Sara Teijeira‐Portas Marta Pengo

Retinal microvascular alterations have been previously described in Parkinson's disease (PD) patients using optical coherence tomography angiography (OCT-A). However, an extensive description of retinal vascular morphological features, their association with PD-related clinical variables and their potential use as diagnostic biomarkers has not been explored.We performed a cross-sectional study including 49 PD patients (87 eyes) and 40 controls (73 eyes). Retinal microvasculature was evaluated with Spectralis OCT-A and cognitive status with Montreal Cognitive Assessment. Unified PD Rating Scale and disease duration were recorded in patients. We extracted microvascular parameters from superficial and deep vascular plexuses of the macula, including the area and circularity of foveal avascular zone (FAZ), skeleton density, perfusion density, vessel perimeter index, vessel mean diameter, fractal dimension (FD) and lacunarity using Python and MATLAB. We compared the microvascular parameters between groups and explored their association with thickness of macular layers and clinical outcomes. Data were analyzed with General Estimating Equations (GEE) and adjusted for age, sex, and hypertension. Logistic regression GEE models were fitted to predict diagnosis of PD versus controls from microvascular, demographic, and clinical data. The discrimination ability of models was tested with receiver operating characteristic curves.FAZ area was significantly smaller in patients compared to controls in superficial and deep plexuses, whereas perfusion density, skeleton density, FD and lacunarity of capillaries were increased in the foveal zone of PD. In the parafovea, microvascular parameters of superficial plexus were associated with ganglion cell-inner plexiform layer thickness, but this was mainly driven by PD with mild cognitive impairment. No such associations were observed in controls. FAZ area was negatively associated with cognition in PD (non-adjusted models). Foveal lacunarity, combined with demographic and clinical confounding factors, yielded an outstanding diagnostic accuracy for discriminating PD patients from controls.Parkinson's disease patients displayed foveal microvascular alterations causing an enlargement of the vascular bed surrounding FAZ. Parafoveal microvascular alterations were less pronounced but were related to inner retinal layer thinning. Retinal microvascular abnormalities helped discriminating PD from controls. All this supports OCT-A as a potential non-invasive biomarker to reveal vascular pathophysiology and improve diagnostic accuracy in PD.

10.3389/fnins.2021.708700

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BundleAtlasing: unbiased population-specific atlasing of bundles in streamline space

Proceedings on CD-ROM - International Society for Magnetic Resonance in Medicine. Scientific Meeting and Exhibition/Proceedings of the International Society for Magnetic Resonance in Medicine, Scientific Meeting and Exhibition (2023)

David Romero-Bascones Bramsh Q. Chandio Shreyas Fadnavis Jong Cheol Park Serge Koudoro

White matter bundle atlases play a crucial role in the segmentation of bundles and the understanding of brain connectomes. However, the construction of streamline atlases that accurately represent the underlying population anatomy is challenging. In this work, we present BundleAtlasing, a new method to compute population-specific bundle atlases in the space of streamlines. The proposed approach is based on two key aspects: an iterative groupwise unbiased bundle registration, and a pairwise bundle combination strategy. We show that our method is able to correctly generate unbiased atlases that represent the average group anatomy of a population.

Bundle adjustment

10.58530/2022/0878

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Association of retinal neurodegeneration with the progression of cognitive decline in Parkinson’s disease

npj Parkinson s Disease (2024)

Ane Murueta‐Goyena David Romero-Bascones Sara Teijeira‐Portas Javier Aritz Urcola Javier Ruiz‐Martínez

Abstract Retinal thickness may serve as a biomarker in Parkinson’s disease (PD). In this prospective longitudinal study, we aimed to determine if PD patients present accelerated thinning rate in the parafoveal ganglion cell-inner plexiform layer (pfGCIPL) and peripapillary retinal nerve fiber layer (pRNFL) compared to controls. Additionally, we evaluated the relationship between retinal neurodegeneration and clinical progression in PD. A cohort of 156 PD patients and 72 controls underwent retinal optical coherence tomography, visual, and cognitive assessments between February 2015 and December 2021 in two Spanish tertiary hospitals. The pfGCIPL thinning rate was twice as high in PD ( β [SE] = −0.58 [0.06]) than in controls ( β [SE] = −0.29 [0.06], p < 0.001). In PD, the progression pattern of pfGCIPL atrophy depended on baseline thickness, with slower thinning rates observed in PD patients with pfGCIPL below 89.8 µm. This result was validated with an external dataset from Moorfields Eye Hospital NHS Foundation Trust (AlzEye study). Slow pfGCIPL progressors, characterized by older at baseline, longer disease duration, and worse cognitive and disease stage scores, showed a threefold increase in the rate of cognitive decline ( β [SE] = −0.45 [0.19] points/year, p = 0.021) compared to faster progressors. Furthermore, temporal sector pRNFL thinning was accelerated in PD ( β time x group [SE] = −0.67 [0.26] μm/year, p = 0.009), demonstrating a close association with cognitive score changes ( β [SE] = 0.11 [0.05], p = 0.052). This study suggests that a slower pattern of pfGCIPL tissue loss in PD is linked to more rapid cognitive decline, whereas changes in temporal pRNFL could track cognitive deterioration.

Cognitive Decline

Inner plexiform layer

10.1038/s41531-024-00637-x

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Citations (7)

Normative thickness maps and foveal pit shapes

Figshare (2022)

David Romero-Bascones

A dataset containing normative macular thickness maps and foveal pit shapes for 444 healthy subjects.

10.6084/m9.figshare.19500548

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Retinal Optical Coherence Tomography Features Associated With Incident and Prevalent Parkinson Disease

Neurology (2023)

Siegfried Wagner David Romero-Bascones Mario Cortina‐Borja Dominic J. Williamson Robbert Struyven

Cadaveric studies have shown disease-related neurodegeneration and other morphological abnormalities in the retina of individuals with Parkinson disease (PD); however, it remains unclear whether this can be reliably detected with in vivo imaging. We investigated inner retinal anatomy, measured using optical coherence tomography (OCT), in prevalent PD and subsequently assessed the association of these markers with the development of PD using a prospective research cohort.

10.1212/wnl.0000000000207727

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Periodontitis and Outer Retinal Thickness: a Cross-Sectional Analysis of the United Kingdom Biobank Cohort

Ophthalmology Science (2024)

Siegfried Wagner Praveen J. Patel Josef Huemer Hagar Khalid Kelsey V. Stuart

PurposePeriodontitis, a ubiquitous severe gum disease affecting the teeth and surrounding alveolar bone can heighten systemic inflammation. We investigated the association between very severe periodontitis and early biomarkers of age-related macular degeneration, in individuals with no eye disease.DesignCross-sectional analysis of the prospective community-based cohort United Kingdom (UK) Biobank.ParticipantsSixty-seven thousand three hundred eleven UK residents aged 40-70 years recruited between 2006-2010 underwent retinal imaging.MethodsMacular-centered optical coherence tomography images acquired at the baseline visit were segmented for retinal sublayer thicknesses. Very severe periodontitis was ascertained through a touchscreen questionnaire. Linear mixed effects regression modeled the association between very severe periodontitis and retinal sublayer thicknesses adjusting for age, sex, ethnicity, socioeconomic status, alcohol consumption, smoking status, diabetes mellitus, hypertension, refractive error, and previous cataract surgery.Main Outcome MeasuresPhotoreceptor layer (PRL) and retinal pigment epithelium-Bruch's membrane (RPE-BM) thicknesses.ResultsAmong 36,897 participants included in the analysis, 1,571 (4.3%) reported very severe periodontitis. Affected individuals were older, lived in areas of greater socioeconomic deprivation and were more likely to be hypertensive, diabetic and current smokers (all p<0.001). On average, those with very severe periodontitis were myopic (-0.29 ± 2.40 diopters) while those unaffected were hyperopic (0.05 ± 2.27 diopters, p<0.001). Following adjusted analysis, very severe periodontitis was associated with thinner PRL (-0.55 μm, 95% CI: -0.97, -0.12, p=0.022) but there was no difference in RPE-BM thickness (0.00 μm, 95% CI: -0.12, 0.13, p=0.97). The association between PRL thickness and very severe periodontitis was modified by age (p<0.001). Stratifying individuals by age, thinner PRL was seen among those aged 60-69 years with disease (-1.19 μm, 95% CI: -1.85, -0.53, p<0.001) but not among those under 60 years.ConclusionsAmong those with no known eye disease, very severe periodontitis is statistically associated with a thinner PRL, consistent with incipient age-related macular degeneration. Optimizing oral hygiene may hold additional relevance for people at risk of degenerative retinal disease.

10.1016/j.xops.2024.100472

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BundleWarp, streamline-based nonlinear registration of white matter tracts

bioRxiv (Cold Spring Harbor Laboratory) (2023)

Bramsh Q. Chandio Emanuele Olivetti David Romero-Bascones Jaroslaw Harezlak Eleftherios Garyfallidis

Abstract Nonlinear registration plays a central role in most neuroimage analysis methods and pipelines, such as in tractography-based individual and group-level analysis methods. However, nonlinear registration is a non-trivial task, especially when dealing with tractography data that digitally represent the underlying anatomy of the brain’s white matter. Furthermore, such process often changes the structure of the data, causing artifacts that can suppress the underlying anatomical and structural details. In this paper, we introduce BundleWarp, a novel and robust streamline-based nonlinear registration method for the registration of white matter tracts. BundleWarp intelligently warps two bundles while preserving the bundles’ crucial topological features. BundleWarp has two main steps. The first step involves the solution of an assignment problem that matches corresponding streamlines from the two bundles (iterLAP step). The second step introduces streamline-specific point-based deformations while keeping the topology of the bundle intact (mlCPD step). We provide comparisons against streamline-based linear registration and image-based nonlinear registration methods. BundleWarp quantitatively and qualitatively outperforms both, and we show that Bundle-Warp can deform and, at the same time, preserve important characteristics of the original anatomical shape of the bundles. Results are shown on 1,728 pairs of bundle registrations across 27 different bundle types. In addition, we present an application of BundleWarp for quantifying bundle shape differences using the generated deformation fields.

Bundle adjustment

Image registration

10.1101/2023.01.04.522802

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Spatial characterization of the effect of age and sex on macular layer thicknesses and foveal pit morphology

PLoS ONE (2022)

David Romero-Bascones Unai Ayala Ane Alberdi Asier Erramuzpe Marta Galdós

Characterizing the effect of age and sex on macular retinal layer thicknesses and foveal pit morphology is crucial to differentiating between natural and disease-related changes. We applied advanced image analysis techniques to optical coherence tomography (OCT) to: 1) enhance the spatial description of age and sex effects, and 2) create a detailed open database of normative retinal layer thickness maps and foveal pit shapes. The maculae of 444 healthy subjects (age range 21–88) were imaged with OCT. Using computational spatial data analysis, thickness maps were obtained for retinal layers and averaged into 400 (20 x 20) sectors. Additionally, the geometry of the foveal pit was radially analyzed by computing the central foveal thickness, rim height, rim radius, and mean slope. The effect of age and sex on these parameters was analyzed with multiple regression mixed-effects models. We observed that the overall age-related decrease of the total retinal thickness (TRT) (-1.1% per 10 years) was mainly driven by the ganglion cell-inner plexiform layer (GCIPL) (-2.4% per 10 years). Both TRT and GCIPL thinning patterns were homogeneous across the macula when using percentual measurements. Although the male retina was 4.1 μm thicker on average, the greatest differences were mainly present for the inner retinal layers in the inner macular ring (up to 4% higher TRT than in the central macula). There was an age-related decrease in the rim height (1.0% per 10 years) and males had a higher rim height, shorter rim radius, and steeper mean slope. Importantly, the radial analysis revealed that these changes are present and relatively uniform across angular directions. These findings demonstrate the capacity of advanced analysis of OCT images to enhance the description of the macula. This, together with the created dataset, could aid the development of more accurate diagnosis models for macular pathologies.

10.1371/journal.pone.0278925

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Foveal Pit Morphology Characterization: A Quantitative Analysis of the Key Methodological Steps

Entropy (2021)

David Romero-Bascones Maitane Barrenechea Ane Murueta‐Goyena Marta Galdós Juan Carlos Gómez‐Esteban

Disentangling the cellular anatomy that gives rise to human visual perception is one of the main challenges of ophthalmology. Of particular interest is the foveal pit, a concave depression located at the center of the retina that captures light from the gaze center. In recent years, there has been a growing interest in studying the morphology of the foveal pit by extracting geometrical features from optical coherence tomography (OCT) images. Despite this, research has devoted little attention to comparing existing approaches for two key methodological steps: the location of the foveal center and the mathematical modelling of the foveal pit. Building upon a dataset of 185 healthy subjects imaged twice, in the present paper the image alignment accuracy of four different foveal center location methods is studied in the first place. Secondly, state-of-the-art foveal pit mathematical models are compared in terms of fitting error, repeatability, and bias. The results indicate the importance of using a robust foveal center location method to align images. Moreover, we show that foveal pit models can improve the agreement between different acquisition protocols. Nevertheless, they can also introduce important biases in the parameter estimates that should be considered.

Microsaccade

10.3390/e23060699

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Citations (3)

Proceedings of the OHBM Brainhack 2021

Aperture Neuro (2023)

Aki Nikolaidis Matteo Manchini Tibor Auer Katherine L. Bottenhorn Eva Alonso‐Ortiz

10.52294/258801b4-a9a9-4d30-a468-c43646391211

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