Cited by 199Multiple Sclerosis Research StudiesAdvanced MRI Techniques and ApplicationsNeuroinflammation and Neurodegeneration Mechanisms

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Quantitative susceptibility mapping identifies inflammation in a subset of chronic multiple sclerosis lesions

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Kaunzner, Ulrike W, Kang, Yeona, Zhang, Shun, Morris, Eric, Yao, Yihao, Pandya, Sneha, Hurtado Rua, Sandra M, Park, Calvin, Gillen, Kelly M, Nguyen, Thanh D, Wang, Yi, Pitt, David, Gauthier, Susan A·2019·Brain

DOI 10.1093/brain/awy296PMC PMC6308309

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Abstract

Chronic active multiple sclerosis lesions, characterized by a hyperintense rim of iron-enriched, activated microglia and macrophages, have been linked to greater tissue damage. Post-mortem studies have determined that chronic active lesions are primarily related to the later stages of multiple sclerosis; however, the occurrence of these lesions, and their relationship to earlier disease stages may be greatly underestimated. Detection of chronic active lesions across the patient spectrum of multiple sclerosis requires a validated imaging tool to accurately identify lesions with persistent inflammation. Quantitative susceptibility mapping provides efficient in vivo quantification of susceptibility changes related to iron deposition and the potential to identify lesions harbouring iron-laden inflammatory cells. The PET tracer 11C-PK11195 targets the translocator protein expressed by activated microglia and infiltrating macrophages. Accordingly, this study aimed to validate that lesions with a hyperintense rim on quantitative susceptibility mapping from both relapsing and progressive patients demonstrate a higher level of innate immune activation as measured on 11C-PK11195 PET. Thirty patients were enrolled in this study, 24 patients had relapsing remitting multiple sclerosis, six had progressive multiple sclerosis, and all patients had concomitant MRI with a gradient echo sequence and PET with 11C-PK11195. A total of 406 chronic lesions were detected, and 43 chronic lesions with a hyperintense rim on quantitative susceptibility mapping were identified as rim+ lesions. Susceptibility (relative to CSF) was higher in rim+ (2.42 ± 17.45 ppb) compared to rim- lesions (-14.6 ± 19.3 ppb, P < 0.0001). Among rim+ lesions, susceptibility within the rim (20.04 ± 14.28 ppb) was significantly higher compared to the core (-5.49 ± 14.44 ppb, P < 0.0001), consistent with the presence of iron. In a mixed-effects model, 11C-PK11195 uptake, representing activated microglia/macrophages, was higher in rim+ lesions compared to rim- lesions (P = 0.015). Validating our in vivo imaging results, multiple sclerosis brain slabs were imaged with quantitative susceptibility mapping and processed for immunohistochemistry. These results showed a positive translocator protein signal throughout the expansive hyperintense border of rim+ lesions, which co-localized with iron containing CD68+ microglia and macrophages. In conclusion, this study provides evidence that suggests that a hyperintense rim on quantitative susceptibility measure within a chronic lesion is a correlate for persistent inflammatory activity and that these lesions can be identified in the relapsing patients. Utilizing quantitative susceptibility measure to differentiate chronic multiple sclerosis lesion subtypes, especially chronic active lesions, would provide a method to assess the impact of these lesions on disease progression.

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Authors: Kaunzner, U. W., Kang, Y., Zhang, S., Morris, E., Yao, Y., Pandya, S., Hurtado Rua, S. M., Park, C., Gillen, K. M., Nguyen, T. D., Wang, Y., Pitt, D., & Gauthier, S. A.
Affiliations: Weill Cornell Medicine (US)
Cornell MRI Research Lab, New York City, NY, USA
Department of Mathematics, College of Sciences and Health Professions, Cleveland State University, Cleveland, OH, USA
Yale University (US)
Corresponding author: Gauthier, Susan A
ORCID: Kaunzner, Ulrike W
Kang, Yeona
Zhang, Shun
Yao, Yihao
Pandya, Sneha
Gillen, Kelly M
Nguyen, Thanh D
Wang, Yi
Pitt, David
Gauthier, Susan A
Venue: Brain
Publisher: Oxford University Press (OUP)
Published: 2018-12-15
Volume: 142
Issue: 1
Pages: 133-145
ISSN: 0006-8950 (ISSN-L)
1460-2156
DOI: 10.1093/brain/awy296
PMC: PMC6308309
OpenAlex: W2904004727
Cited by: 199
References: 63
Citations by year: 2026: 15 · 2025: 20 · 2024: 40 · 2023: 27 · 2022: 33 · 2021: 30 · 2020: 23 · 2019: 11
FWCI: 12.17
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor, 1 d)
Locations: Brain (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
EngagedScholarship @ Cleveland State University (Cleveland State University) (submittedVersion)
Funders: National Institutes of Health (RO1 NS090464)
Biogen (55000025)
Genzyme (56585757)
Novartis (56585786, UL1 TR000456-06)
Weill Cornell Clinical and Translational Science Center
Topics: Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: chronic active lesions, quantitative susceptibility mapping, [11C]PK11195, translocator protein (TSPO), microglial activation, macrophages, iron accumulation, innate immune activation, relapsing-remitting multiple sclerosis, progressive multiple sclerosis, CD68, immunohistochemistry
MeSH terms: CD68 Molecule, Adult, Aged, Brain, Carbon Radioisotopes, Chronic Disease, Cross-Sectional Studies, Female, Humans, Inflammation, Iron, Isoquinolines, Macrophages, Magnetic Resonance Imaging, Male, Middle Aged, Multiple Sclerosis, Retrospective Studies, Antigens, Differentiation, Myelomonocytic, Antigens, CD, Microglia, Positron-Emission Tomography, Young Adult

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Quantitative susceptibility mapping identifies inflammation in a subset of chronic multiple sclerosis lesions

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