The Sense of Smell ( SoS ) Atlas: Its Creation and First Application to Investigate COVID ‐19 Related Anosmia With a Comprehensive Quantitative MRI Protocol
The loss of smell, that is, anosmia, is a common symptom in COVID‐19, but the brain alterations behind it are still unclear. In this study, researchers developed the Sense of Smell (SoS) atlas, a new tool that included parts of the brain involved in olfaction. They applied the atlas to advanced MRI...
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03.10.2025
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| Abstract | The loss of smell, that is, anosmia, is a common symptom in COVID‐19, but the brain alterations behind it are still unclear. In this study, researchers developed the Sense of Smell (SoS) atlas, a new tool that included parts of the brain involved in olfaction. They applied the atlas to advanced MRI metrics of participants with persistent smell loss, participants who had recovered, and healthy controls. Results showed signs of neuroinflammation and axonal damage in persistent anosmia, and myelin changes in recovered anosmia. The SoS atlas provides a valuable tool to study smell‐related brain changes in COVID‐19 and other diseases. |
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| AbstractList | The loss of smell (anosmia) has been noted in numerous diseases, including COVID-19. Inflammatory and microstructural alterations are possible underlying mechanisms of anosmia in COVID-19. However, no atlas exists to study olfaction and the associated tissue property changes.
To develop the sense of smell (SoS) atlas, including gray matter regions and white matter tracts of the olfactory circuit, to investigate the underpinnings of COVID-19 related anosmia.
Retrospective.
For the SoS atlas, high-resolution tractograms of 10 healthy controls (HC) of the Human Connectome Project (7 females, 22-35 years) were used. The SoS atlas was applied to 8 subjects with persistent anosmia following COVID-19 (COVID-P, 7 females, 52 ± 12 years), 19 subjects that recovered from COVID-19 anosmia (COVID-R, 14 females, 38 ± 13 years), and 17 HC (8 females, 39 ± 12 years).
3 T, 3D inversion recovery, 3D fast field echo, and spin-echo echo-planar imaging sequences.
To create the SoS atlas, regions were identified and tracts were extracted via tractography following biological constraints. MRI metrics sensitive to alterations in neuroinflammation, axonal degeneration, myelin and macromolecular density, and iron were analyzed.
Region-based analysis (p-value < 0.05, false discovery rate (FDR) corrected) and voxel-based analysis (p-value < 0.001 uncorrected, FDR-corrected cluster extent = 5 voxels) were performed on 15 multisequence-MRI metrics between the three groups.
The SoS atlas consisted of 35 regions and, after anatomical curation, the initial 506 tracts were refined to 78. Compared to HC, COVID-P presented alterations in neuroinflammation-related (mean: 41% of total alterations) and axonal degeneration-related (31%) MRI metrics, while COVID-R presented alterations of myelin-related metrics (68%). COVID-P alterations mainly affected the hindbrain (56%), while COVID-R the hindbrain (39%).
A novel tool, the SoS atlas, was developed to study the olfactory system and applied in combination with multisequence-MRI metrics to investigate the mechanisms of COVID-19 related anosmia.
3.
Stage 1. The loss of smell, that is, anosmia, is a common symptom in COVID‐19, but the brain alterations behind it are still unclear. In this study, researchers developed the Sense of Smell (SoS) atlas, a new tool that included parts of the brain involved in olfaction. They applied the atlas to advanced MRI metrics of participants with persistent smell loss, participants who had recovered, and healthy controls. Results showed signs of neuroinflammation and axonal damage in persistent anosmia, and myelin changes in recovered anosmia. The SoS atlas provides a valuable tool to study smell‐related brain changes in COVID‐19 and other diseases. The loss of smell (anosmia) has been noted in numerous diseases, including COVID-19. Inflammatory and microstructural alterations are possible underlying mechanisms of anosmia in COVID-19. However, no atlas exists to study olfaction and the associated tissue property changes.BACKGROUNDThe loss of smell (anosmia) has been noted in numerous diseases, including COVID-19. Inflammatory and microstructural alterations are possible underlying mechanisms of anosmia in COVID-19. However, no atlas exists to study olfaction and the associated tissue property changes.To develop the sense of smell (SoS) atlas, including gray matter regions and white matter tracts of the olfactory circuit, to investigate the underpinnings of COVID-19 related anosmia.PURPOSETo develop the sense of smell (SoS) atlas, including gray matter regions and white matter tracts of the olfactory circuit, to investigate the underpinnings of COVID-19 related anosmia.Retrospective.STUDY TYPERetrospective.For the SoS atlas, high-resolution tractograms of 10 healthy controls (HC) of the Human Connectome Project (7 females, 22-35 years) were used. The SoS atlas was applied to 8 subjects with persistent anosmia following COVID-19 (COVID-P, 7 females, 52 ± 12 years), 19 subjects that recovered from COVID-19 anosmia (COVID-R, 14 females, 38 ± 13 years), and 17 HC (8 females, 39 ± 12 years).SUBJECTSFor the SoS atlas, high-resolution tractograms of 10 healthy controls (HC) of the Human Connectome Project (7 females, 22-35 years) were used. The SoS atlas was applied to 8 subjects with persistent anosmia following COVID-19 (COVID-P, 7 females, 52 ± 12 years), 19 subjects that recovered from COVID-19 anosmia (COVID-R, 14 females, 38 ± 13 years), and 17 HC (8 females, 39 ± 12 years).3 T, 3D inversion recovery, 3D fast field echo, and spin-echo echo-planar imaging sequences.FIELD STRENGTH/SEQUENCE3 T, 3D inversion recovery, 3D fast field echo, and spin-echo echo-planar imaging sequences.To create the SoS atlas, regions were identified and tracts were extracted via tractography following biological constraints. MRI metrics sensitive to alterations in neuroinflammation, axonal degeneration, myelin and macromolecular density, and iron were analyzed.ASSESSMENTTo create the SoS atlas, regions were identified and tracts were extracted via tractography following biological constraints. MRI metrics sensitive to alterations in neuroinflammation, axonal degeneration, myelin and macromolecular density, and iron were analyzed.Region-based analysis (p-value < 0.05, false discovery rate (FDR) corrected) and voxel-based analysis (p-value < 0.001 uncorrected, FDR-corrected cluster extent = 5 voxels) were performed on 15 multisequence-MRI metrics between the three groups.STATISTICAL TESTSRegion-based analysis (p-value < 0.05, false discovery rate (FDR) corrected) and voxel-based analysis (p-value < 0.001 uncorrected, FDR-corrected cluster extent = 5 voxels) were performed on 15 multisequence-MRI metrics between the three groups.The SoS atlas consisted of 35 regions and, after anatomical curation, the initial 506 tracts were refined to 78. Compared to HC, COVID-P presented alterations in neuroinflammation-related (mean: 41% of total alterations) and axonal degeneration-related (31%) MRI metrics, while COVID-R presented alterations of myelin-related metrics (68%). COVID-P alterations mainly affected the hindbrain (56%), while COVID-R the hindbrain (39%).RESULTSThe SoS atlas consisted of 35 regions and, after anatomical curation, the initial 506 tracts were refined to 78. Compared to HC, COVID-P presented alterations in neuroinflammation-related (mean: 41% of total alterations) and axonal degeneration-related (31%) MRI metrics, while COVID-R presented alterations of myelin-related metrics (68%). COVID-P alterations mainly affected the hindbrain (56%), while COVID-R the hindbrain (39%).A novel tool, the SoS atlas, was developed to study the olfactory system and applied in combination with multisequence-MRI metrics to investigate the mechanisms of COVID-19 related anosmia.DATA CONCLUSIONA novel tool, the SoS atlas, was developed to study the olfactory system and applied in combination with multisequence-MRI metrics to investigate the mechanisms of COVID-19 related anosmia.3.EVIDENCE LEVEL3.Stage 1.TECHNICAL EFFICACYStage 1. |
| Author | Kanber, Baris Monteverdi, Anita Palesi, Fulvia Gaviraghi, Marta Battiston, Marco Prados Carrasco, Ferran Grussu, Francesco Gandini Wheeler‐Kingshott, Claudia A. M. Yiannakas, Marios C. D'Angelo, Egidio Grosso, Elena Baiguera, Mattia Batterham, Rachel L. Fusari, Andrea Makaronidis, Janine Zandi, Michael S. Samson, Rebecca S. Lupi, Eleonora |
| Author_xml | – sequence: 1 givenname: Marta orcidid: 0000-0001-7427-845X surname: Gaviraghi fullname: Gaviraghi, Marta organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy – sequence: 2 givenname: Eleonora orcidid: 0009-0001-4519-8888 surname: Lupi fullname: Lupi, Eleonora organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy – sequence: 3 givenname: Elena surname: Grosso fullname: Grosso, Elena organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy – sequence: 4 givenname: Andrea surname: Fusari fullname: Fusari, Andrea organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy – sequence: 5 givenname: Mattia surname: Baiguera fullname: Baiguera, Mattia organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy – sequence: 6 givenname: Anita surname: Monteverdi fullname: Monteverdi, Anita organization: Digital Neuroscience Centre IRCCS Mondino Foundation Pavia Italy – sequence: 7 givenname: Marco surname: Battiston fullname: Battiston, Marco organization: NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK, ASG Superconductors s.p.a. Genova Italy – sequence: 8 givenname: Francesco surname: Grussu fullname: Grussu, Francesco organization: NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK, Radiomics Group, Vall d'Hebron Institute of Oncology Vall d'Hebron Barcelona Hospital Campus Barcelona Spain – sequence: 9 givenname: Baris surname: Kanber fullname: Kanber, Baris organization: NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK, Department of Medical Physics and Biomedical Engineering, UCL Hawkes Institute University College London London UK – sequence: 10 givenname: Ferran orcidid: 0000-0002-7872-0142 surname: Prados Carrasco fullname: Prados Carrasco, Ferran organization: NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK, Department of Medical Physics and Biomedical Engineering, UCL Hawkes Institute University College London London UK, E‐Health Center Universitat Oberta de Catalunya Barcelona Spain – sequence: 11 givenname: Rebecca S. surname: Samson fullname: Samson, Rebecca S. organization: NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK – sequence: 12 givenname: Janine surname: Makaronidis fullname: Makaronidis, Janine organization: Centre for Obesity Research, Department of Medicine University College London London UK, National Institute of Health Research UCLH Biomedical Research Centre London UK, Department of Diabetes and Metabolism, Royal London Hospital Barts Health NHS Trust London UK – sequence: 13 givenname: Marios C. surname: Yiannakas fullname: Yiannakas, Marios C. organization: NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK – sequence: 14 givenname: Michael S. surname: Zandi fullname: Zandi, Michael S. organization: Department of Neuroinflammation UCL Queen Square Institute of Neurology London UK – sequence: 15 givenname: Rachel L. surname: Batterham fullname: Batterham, Rachel L. organization: Centre for Obesity Research, Department of Medicine University College London London UK, National Institute of Health Research UCLH Biomedical Research Centre London UK – sequence: 16 givenname: Egidio surname: D'Angelo fullname: D'Angelo, Egidio organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy, Digital Neuroscience Centre IRCCS Mondino Foundation Pavia Italy – sequence: 17 givenname: Fulvia surname: Palesi fullname: Palesi, Fulvia organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy – sequence: 18 givenname: Claudia A. M. orcidid: 0000-0002-4832-1300 surname: Gandini Wheeler‐Kingshott fullname: Gandini Wheeler‐Kingshott, Claudia A. M. organization: Department of Brain and Behavioral Sciences University of Pavia Pavia Italy, Digital Neuroscience Centre IRCCS Mondino Foundation Pavia Italy, NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK |
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| Keywords | multisequence‐MRI tractography hindbrain neuroinflammation and myelin alterations COVID‐19 anosmia sense of smell atlas |
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| Snippet | The loss of smell, that is, anosmia, is a common symptom in COVID‐19, but the brain alterations behind it are still unclear. In this study, researchers... The loss of smell (anosmia) has been noted in numerous diseases, including COVID-19. Inflammatory and microstructural alterations are possible underlying... |
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| Title | The Sense of Smell ( SoS ) Atlas: Its Creation and First Application to Investigate COVID ‐19 Related Anosmia With a Comprehensive Quantitative MRI Protocol |
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