Investigating morphological changes in the brain in relation to etiology and duration of olfactory dysfunction with voxel-based morphometry

Postma, Elbrich M.; Smeets, Paul A.M.; Boek, Wilbert M.; Boesveldt, Sanne

doi:10.1038/s41598-021-92224-w

Cited by 15 publications

(13 citation statements)

References 57 publications

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“…A more extensive study of congenital and acquired (post-infectious, chronic inflammation due to rhinosinusitis, or idiopathic) olfactory loss also demonstrated an association between grey matter volume and olfactory function in the orbitofrontal cortex 17 . It also showed that duration of olfactory loss for those with acquired olfactory dysfunction, ranging from 0 to over 10 years, was related to more pronounced loss of grey matter in the gyrus rectus and orbitofrontal cortex 17 . On the other hand, it has been reported in a longitudinal study that patients with idiopathic olfactory loss had higher grey matter volume after undergoing olfactory training in various brain regions including the orbitofrontal cortex and gyrus rectus 42 .…”

Section: Discussionmentioning

confidence: 92%

“…In a recent study, 100% of the patients in the subacute stage of the disease were displaying signs of gustatory impairment (hypogeusia), and 86% either hyposmia or anosmia 16 . Such loss of sensory olfactory inputs to the brain could lead to a loss of grey matter in olfactory-related brain regions 17 . Olfactory — whether neuronal or supporting — cells concentrated in the olfactory epithelium are also particularly vulnerable to coronavirus invasion, and this seems to be also the case specifically with SARS-CoV-2 15,18–20 .…”

mentioning

confidence: 99%

“…These large numbers may allow us to detect subtle, but consistent spatially distributed sites of damage associated with the infection, thus underlining in vivo the possible spreading pathways of the effects of the disease within the brain (whether such effects relate to the invasion of the virus itself 11,18 doi.org/10.21203/rs.3.rs-1139035/v1, inflammatory reactions 3,4 doi.org/10.1101/2021. 02.23.432474, possible anterograde degeneration starting with the olfactory neurons in the nose, or through sensory deprivation 17,26,27 ). The longitudinal aspect of the study aims to help tease apart which of the observed effects between first and second scans are likely related to the infection, rather than due to pre-existing risk factors between the two groups.…”

mentioning

confidence: 99%

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SARS-CoV-2 is associated with changes in brain structure in UK Biobank

Douaud

Lee

Alfaro-Almagro

et al. 2021

Preprint

144

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There is strong evidence for brain-related pathologies in COVID-19, some of which could be a consequence of viral neurotropism. The vast majority of brain imaging studies so far have focused on qualitative, gross pathology of moderate to severe cases, often carried out on hospitalised patients. It remains unknown however whether the impact of COVID-19 can be detected in milder cases, in a quantitative and automated manner, and whether this can reveal a possible mechanism for the spread of the disease. UK Biobank scanned over 40,000 participants before the start of the COVID-19 pandemic, making it possible to invite back in 2021 hundreds of previously-imaged participants for a second imaging visit. Here, we studied the effects of the disease in the brain using multimodal data from 782 participants from the UK Biobank COVID-19 re-imaging study, with 394 participants having tested positive for SARS- CoV-2 infection between their two scans. We used structural and functional brain scans from before and after infection, to compare longitudinal brain changes between these 394 COVID- 19 patients and 388 controls who were matched for age, sex, ethnicity and interval between scans. We identified significant effects of COVID-19 in the brain with a loss of grey matter in the left parahippocampal gyrus, the left lateral orbitofrontal cortex and the left insula. When looking over the entire cortical surface, these results extended to the anterior cingulate cortex, supramarginal gyrus and temporal pole. We further compared COVID-19 patients who had been hospitalised (n=15) with those who had not (n=379), and while results were not significant, we found comparatively similar findings to the COVID-19 vs control group comparison, with, in addition, a greater loss of grey matter in the cingulate cortex, central nucleus of the amygdala and hippocampal cornu ammonis (all |Z|>3). Our findings thus consistently relate to loss of grey matter in limbic cortical areas directly linked to the primary olfactory and gustatory system. Unlike in post hoc disease studies, the availability of pre- infection imaging data helps avoid the danger of pre-existing risk factors or clinical conditions being mis-interpreted as disease effects. Since a possible entry point of the virus to the central nervous system might be via the olfactory mucosa and the olfactory bulb, these brain imaging results might be the in vivo hallmark of the spread of the disease (or the virus itself) via olfactory and gustatory pathways.

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Section: Discussionmentioning

confidence: 92%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

SARS-CoV-2 is associated with changes in brain structure in UK Biobank

Douaud

Lee

Alfaro-Almagro

et al. 2021

Preprint

144

View full text Add to dashboard Cite

show abstract

“…These large numbers may allow us to detect subtle, but consistent spatially distributed sites of damage associated with the infection, thus underlining in vivo the possible spreading pathways of the effects of the disease within the brain (whether such effects relate to the invasion of the virus itself 11,18 https:// doi.org/10.21203/rs.3.rs-1139035/v1, inflammatory reactions 3,4 https:// doi.org/10.1101/2021.02. 23.432474, possible anterograde degeneration starting with the olfactory neurons in the nose, or through sensory deprivation 17,26,27 ). The longitudinal aspect of the study aims to help tease apart which of the observed effects between first and second scans are likely related to the infection, rather than due to pre-existing risk factors between the two groups.…”

Section: Articlementioning

confidence: 99%

“…In a recent study, 100% of the patients in the subacute stage of the disease were displaying signs of gustatory impairment (hypogeusia), and 86% either hyposmia or anosmia 16 . Such loss of sensory olfactory inputs to the brain could lead to a loss of grey matter in olfactory-related brain regions 17 . Olfactorywhether neuronal or supporting -cells concentrated in the olfactory epithelium are also particularly vulnerable to coronavirus invasion, and this seems to be also the case specifically with SARS-CoV-2 15,[18][19][20] .…”

mentioning

confidence: 99%

SARS-CoV-2 is associated with changes in brain structure in UK Biobank

Douaud

Lee

Alfaro-Almagro

et al. 2022

Nature

1,133

892

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This is a PDF file of a peer-reviewed paper that has been accepted for publication. Although unedited, the content has been subjected to preliminary formatting. Nature is providing this early version of the typeset paper as a service to our authors and readers. The text and figures will undergo copyediting and a proof review before the paper is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers apply.

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MRI evidence of gray matter loss in COVID‐19 patients with cognitive and olfactory disorders

Capelli,

Arrigoni,

Napolitano

et al. 2024

Ann Clin Transl Neurol

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ObjectiveThe aim of this study was to assess COVID‐19‐related gray matter (GM) structural alterations in two distinct groups of patients presenting with the prevailing and distinctive COVID‐19‐related neurological symptoms – isolated olfactory disorders as sole neurological manifestation (COVID‐OD) and cognitive disorders (COVID‐CD) – as compared to a control group of unaffected individuals.MethodsThe study included 61 COVID‐CD patients (57 [60–63] years, 62% females), 84 COVID‐OD patients (49 [35–57] years, 60% females), and 17 controls (51 [41–52] years, 41% females). Region‐based morphometry (RBM) and voxel‐based morphometry (VBM) were performed on T1‐weighted MRI scans to assess GM regional volume and voxel‐wise density differences between COVID‐19 patients and controls. Surface‐based morphometry (SBM) was applied to investigate cortical thickness alterations. The statistical models built to assess GM structural differences among groups included total intracranial volume and age as nuisance variables.ResultsThe multi‐morphometric analysis revealed statistically significant (p < 0.05 corrected for multiple comparisons) reduction in GM regional volumes, in voxel‐wise GM density and in cortical thickness in both COVID‐CD and COVID‐OD patient groups as compared to controls. Across all three analyses, COVID‐CD patients showed more distributed and severe GM loss than COVID‐OD patients. The most prominently affected GM regions in the COVID‐CD group included the hippocampus, putamen, cingulate gyrus, precuneus, precentral and postcentral gyri, amygdala, lingual gyrus, and caudate nucleus.InterpretationOur MRI findings show that COVID‐19‐related olfactory and cognitive disorders both induce GM atrophy, although at different degrees of severity, likely indicative of neurodegeneration and neuroinflammation.

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Investigating morphological changes in the brain in relation to etiology and duration of olfactory dysfunction with voxel-based morphometry

Cited by 15 publications

References 57 publications

SARS-CoV-2 is associated with changes in brain structure in UK Biobank

SARS-CoV-2 is associated with changes in brain structure in UK Biobank

SARS-CoV-2 is associated with changes in brain structure in UK Biobank

MRI evidence of gray matter loss in COVID‐19 patients with cognitive and olfactory disorders

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