Quantitative susceptibility mapping at 7 T in COVID-19: brainstem effects and outcome associations
Post-mortem studies have shown that patients dying from severe acute respiratory syndrome coronavirus (SARS-CoV-2) infection frequently have pathological changes in their CNS, particularly in the brainstem. Many of these changes are proposed to result from para-infectious and/or post-infection immune responses. Clinical symptoms such as fatigue, breathlessness, and chest pain are frequently reported in post-hospitalized coronavirus disease 2019 (COVID-19) patients. We propose that these symptoms are in part due to damage to key neuromodulatory brainstem nuclei. While brainstem involvement has been demonstrated in the acute phase of the illness, the evidence of long-term brainstem change on MRI is inconclusive. We therefore used ultra-high field (7 T) quantitative susceptibility mapping (QSM) to test the hypothesis that brainstem abnormalities persist in post-COVID patients and that these are associated with persistence of key symptoms. We used 7 T QSM data from 30 patients, scanned 93-548 days after hospital admission for COVID-19 and compared them to 51 age-matched controls without prior history of COVID-19 infection. We correlated the patients' QSM signals with disease severity (duration of hospital admission and COVID-19 severity scale), inflammatory response during the acute illness (C-reactive protein, D-dimer and platelet levels), functional recovery (modified Rankin scale), depression (Patient Health Questionnaire-9) and anxiety (Generalized Anxiety Disorder-7). In COVID-19 survivors, the MR susceptibility increased in the medulla, pons and midbrain regions of the brainstem. Specifically, there was increased susceptibility in the inferior medullary reticular formation and the raphe pallidus and obscurus. In these regions, patients with higher tissue susceptibility had worse acute disease severity, higher acute inflammatory markers, and significantly worse functional recovery. This study contributes to understanding the long-term effects of COVID-19 and recovery. Using non-invasive ultra-high field 7 T MRI, we show evidence of brainstem pathophysiological changes associated with inflammatory processes in post-hospitalized COVID-19 survivors.
Authors
- Christopher T. Rodgers (ORCID: https://orcid.org/0000-0003-1275-1197)
- Emmanuel Andreas Stamatakis (ORCID: https://orcid.org/0000-0001-6955-9601)
- Stuart Clare
- Karen D. Ersche (ORCID: https://orcid.org/0000-0002-3203-1878)
- James B. Rowe (ORCID: https://orcid.org/0000-0001-7216-8679)
- Victoria Lupson
- William T. Clarke (ORCID: https://orcid.org/0000-0001-7159-7025)
- Betty Raman (ORCID: https://orcid.org/0000-0002-1239-9608)
- Martyn Ezra (ORCID: https://orcid.org/0000-0002-6262-5247)
- Guy Williams (ORCID: https://orcid.org/0000-0001-5223-6654)
- Edward Thomas Bullmore (ORCID: https://orcid.org/0000-0002-8955-8283)
- Lin Qiu (ORCID: https://orcid.org/0000-0001-8419-1833)
- David Krishna Menon (ORCID: https://orcid.org/0000-0002-3228-9692)
- Doris A. Chatfield
- Anne E. Manktelow (ORCID: https://orcid.org/0000-0002-2319-1669)
- Virginia Newcombe (ORCID: https://orcid.org/0000-0001-6044-9035)
- Stephen Sawcer (ORCID: https://orcid.org/0000-0001-7685-0974)
- Stefan Neubauer (ORCID: https://orcid.org/0000-0001-9017-5645)
- Joanne Outtrim (ORCID: https://orcid.org/0000-0001-8118-6430)
- Kyle T.S. Pattinson (ORCID: https://orcid.org/0000-0003-1353-2199)
- Mark Philip Cassar (ORCID: https://orcid.org/0000-0001-7192-6917)
- Rory McDonald (ORCID: https://orcid.org/0009-0005-4241-5065)
- Catarina Rua (ORCID: https://orcid.org/0000-0002-0404-4399)
Institutions
- MRC Cognition and Brain Sciences Unit (GB)
- Heidelberg University (DE)
- University of Cambridge (GB)
- University of Oxford (GB)
- Invicro (United Kingdom) (GB)
- Wellcome Centre for Integrative Neuroimaging (GB)
- Central Institute of Mental Health (DE)
- Oxford University Hospitals NHS Trust (GB)
- Imaging Center (US)
- Imperial College London (GB)
- Medical Research Council (GB)
Publication Details
- Journal
- Brain
- Published
- 2024-10-07
- DOI
- https://doi.org/10.1093/brain/awae215
- Citations
- 31
- Primary Topic
- Long-Term Effects of COVID-19
- Type
- article
- Field-Weighted Citation Impact
- 11.44
Funders
- National Institute on Handicapped Research
- NHS Blood and Transplant
- Wellcome Trust
- National Institute for Health and Care Research
- British Heart Foundation
- Department of Health and Social Care
- University of Oxford
- BHF Centre of Research Excellence, Oxford
- Medical Research Council Canada
- NIHR BioResource
- Medical Research Council
- NIHR Oxford Biomedical Research Centre
- NIHR Cambridge Biomedical Research Centre
- Cambridge Centre for Parkinson-Plus