Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context

Summary: Background: Olfactory impairments and anosmia from COVID-19 infection typically resolve within 2–4 weeks, although in some cases, symptoms persist longer. COVID-19-related anosmia is associated with olfactory bulb atrophy, however, the impact on cortical structures is relatively unknown, p...

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Main Authors: Jed Wingrove, Janine Makaronidis, Ferran Prados, Baris Kanber, Marios C. Yiannakas, Cormac Magee, Gloria Castellazzi, Louis Grandjean, Xavier Golay, Carmen Tur, Olga Ciccarelli, Egidio D'Angelo, Claudia A.M. Gandini Wheeler-Kingshott, Rachel L. Batterham
Format: Article
Language:English
Published: Elsevier 2023-04-01
Series:EClinicalMedicine
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589537023000603
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author Jed Wingrove
Janine Makaronidis
Ferran Prados
Baris Kanber
Marios C. Yiannakas
Cormac Magee
Gloria Castellazzi
Louis Grandjean
Xavier Golay
Carmen Tur
Olga Ciccarelli
Egidio D'Angelo
Claudia A.M. Gandini Wheeler-Kingshott
Rachel L. Batterham
author_facet Jed Wingrove
Janine Makaronidis
Ferran Prados
Baris Kanber
Marios C. Yiannakas
Cormac Magee
Gloria Castellazzi
Louis Grandjean
Xavier Golay
Carmen Tur
Olga Ciccarelli
Egidio D'Angelo
Claudia A.M. Gandini Wheeler-Kingshott
Rachel L. Batterham
author_sort Jed Wingrove
collection DOAJ
description Summary: Background: Olfactory impairments and anosmia from COVID-19 infection typically resolve within 2–4 weeks, although in some cases, symptoms persist longer. COVID-19-related anosmia is associated with olfactory bulb atrophy, however, the impact on cortical structures is relatively unknown, particularly in those with long-term symptoms. Methods: In this exploratory, observational study, we studied individuals who experienced COVID-19-related anosmia, with or without recovered sense of smell, and compared against individuals with no prior COVID-19 infection (confirmed by antibody testing, all vaccine naïve). MRI Imaging was carried out between the 15th July and 17th November 2020 at the Queen Square House Clinical Scanning Facility, UCL, United Kingdom. Using functional magnetic resonance imaging (fMRI) and structural imaging, we assessed differences in functional connectivity (FC) between olfactory regions, whole brain grey matter (GM) cerebral blood flow (CBF) and GM density. Findings: Individuals with anosmia showed increased FC between the left orbitofrontal cortex (OFC), visual association cortex and cerebellum and FC reductions between the right OFC and dorsal anterior cingulate cortex compared to those with no prior COVID-19 infection (p < 0.05, from whole brain statistical parametric map analysis). Individuals with anosmia also showed greater CBF in the left insula, hippocampus and ventral posterior cingulate when compared to those with resolved anosmia (p < 0.05, from whole brain statistical parametric map analysis). Interpretation: This work describes, for the first time to our knowledge, functional differences within olfactory areas and regions involved in sensory processing and cognitive functioning. This work identifies key areas for further research and potential target sites for therapeutic strategies. Funding: This study was funded by the National Institute for Health and Care Research and supported by the Queen Square Scanner business case.
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spelling doaj.art-ecb0e15a1cdb46d0bad51af43ee93af92023-03-04T04:23:44ZengElsevierEClinicalMedicine2589-53702023-04-0158101883Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in contextJed Wingrove0Janine Makaronidis1Ferran Prados2Baris Kanber3Marios C. Yiannakas4Cormac Magee5Gloria Castellazzi6Louis Grandjean7Xavier Golay8Carmen Tur9Olga Ciccarelli10Egidio D'Angelo11Claudia A.M. Gandini Wheeler-Kingshott12Rachel L. Batterham13Centre for Obesity Research, Department of Medicine, University College London, London, UK; National Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UKCentre for Obesity Research, Department of Medicine, University College London, London, UK; National Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UKNational Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UK; NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK; Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, UKNational Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UK; NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK; Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, UKNMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UKCentre for Obesity Research, Department of Medicine, University College London, London, UK; National Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UKNMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK; Brain Connectivity Research Centre, IRCCS Mondino Foundation, Pavia, ItalyDepartment of Infection, Immunity &amp; Inflammation, UCL Great Ormond Street Institute of Child Health, University College London, London, UKNMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK; Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of Neurology, University College London, London, UKNMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UKNational Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UK; NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UKBrain Connectivity Research Centre, IRCCS Mondino Foundation, Pavia, Italy; Department of Brain and Behavioural Sciences, University of Pavia, Pavia, ItalyNMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, University College London, London, UK; Brain Connectivity Research Centre, IRCCS Mondino Foundation, Pavia, Italy; Department of Brain and Behavioural Sciences, University of Pavia, Pavia, ItalyCentre for Obesity Research, Department of Medicine, University College London, London, UK; National Institute for Health and Care Research, Biomedical Research Centre at UCLH and UCL, London, UK; Corresponding author. Division of Medicine, University College London, Rayne Building, 5 University Street, London, WC1E 6JF, UK.Summary: Background: Olfactory impairments and anosmia from COVID-19 infection typically resolve within 2–4 weeks, although in some cases, symptoms persist longer. COVID-19-related anosmia is associated with olfactory bulb atrophy, however, the impact on cortical structures is relatively unknown, particularly in those with long-term symptoms. Methods: In this exploratory, observational study, we studied individuals who experienced COVID-19-related anosmia, with or without recovered sense of smell, and compared against individuals with no prior COVID-19 infection (confirmed by antibody testing, all vaccine naïve). MRI Imaging was carried out between the 15th July and 17th November 2020 at the Queen Square House Clinical Scanning Facility, UCL, United Kingdom. Using functional magnetic resonance imaging (fMRI) and structural imaging, we assessed differences in functional connectivity (FC) between olfactory regions, whole brain grey matter (GM) cerebral blood flow (CBF) and GM density. Findings: Individuals with anosmia showed increased FC between the left orbitofrontal cortex (OFC), visual association cortex and cerebellum and FC reductions between the right OFC and dorsal anterior cingulate cortex compared to those with no prior COVID-19 infection (p < 0.05, from whole brain statistical parametric map analysis). Individuals with anosmia also showed greater CBF in the left insula, hippocampus and ventral posterior cingulate when compared to those with resolved anosmia (p < 0.05, from whole brain statistical parametric map analysis). Interpretation: This work describes, for the first time to our knowledge, functional differences within olfactory areas and regions involved in sensory processing and cognitive functioning. This work identifies key areas for further research and potential target sites for therapeutic strategies. Funding: This study was funded by the National Institute for Health and Care Research and supported by the Queen Square Scanner business case.http://www.sciencedirect.com/science/article/pii/S2589537023000603COVID-19 anosmiaOlfactory impairmentsFunctional neuroimagingOlfactory networksResting state connectivityCerebral blood flow
spellingShingle Jed Wingrove
Janine Makaronidis
Ferran Prados
Baris Kanber
Marios C. Yiannakas
Cormac Magee
Gloria Castellazzi
Louis Grandjean
Xavier Golay
Carmen Tur
Olga Ciccarelli
Egidio D'Angelo
Claudia A.M. Gandini Wheeler-Kingshott
Rachel L. Batterham
Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context
EClinicalMedicine
COVID-19 anosmia
Olfactory impairments
Functional neuroimaging
Olfactory networks
Resting state connectivity
Cerebral blood flow
title Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context
title_full Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context
title_fullStr Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context
title_full_unstemmed Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context
title_short Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational studyResearch in context
title_sort aberrant olfactory network functional connectivity in people with olfactory dysfunction following covid 19 infection an exploratory observational studyresearch in context
topic COVID-19 anosmia
Olfactory impairments
Functional neuroimaging
Olfactory networks
Resting state connectivity
Cerebral blood flow
url http://www.sciencedirect.com/science/article/pii/S2589537023000603
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