Limbic system damage in MS: MRI assessment and correlations with clinical testing

PLoS One. 2017 Nov 9;12(11):e0187915. doi: 10.1371/journal.pone.0187915. eCollection 2017.

Abstract

Volume loss in some limbic region structures has been observed in multiple sclerosis (MS) patients. However, in vivo evaluation of existing tissue cellular microstructure integrity has received less attention. The goal of studies reported here was to quantitatively assess loss of limbic system volumes and tissue integrity, and to evaluate associations of these measures with cognitive and physical dysfunction in MS patients. Thirty-one healthy controls (HC) and 80 MS patients, including 32 relapsing remitting (RRMS), 32 secondary progressive (SPMS) and 16 primary progressive (PPMS), participated in this study. Tissue cellular integrity was evaluated by means of recently introduced tissue-specific parameter R2t* that was calculated from multi-gradient-echo MRI signals using a recently developed method that separates R2t* from BOLD (blood oxygen level dependent) contributions to GRE signal decay rate constant (R2*), and accounting for physiological fluctuations and artifacts from background gradients. Volumes in limbic system regions, normalized to skull size (NV), were measured from standard MPRAGE images. MS patients had lower R2t* and smaller normalized volumes in the hippocampus, amygdala, and several other limbic system regions, compared to HC. Alterations in R2t* of several limbic system regions correlated with clinical and neurocognitive test scores in MS patients. In contrast, smaller normalized volumes in MS were only correlated with neurocognitive test scores in the hippocampus and amygdala. This study reports the novel finding that R2t*, a measure that estimates tissue integrity, is more sensitive to tissue damage in limbic system structures than is atrophy. R2t* measurements can serve as a biomarker that is distinct from and complementary to volume measurements.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Female
  • Humans
  • Limbic System / diagnostic imaging
  • Limbic System / pathology*
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Multiple Sclerosis, Chronic Progressive / diagnostic imaging*
  • Multiple Sclerosis, Chronic Progressive / pathology
  • Multiple Sclerosis, Chronic Progressive / psychology*
  • Multiple Sclerosis, Relapsing-Remitting / diagnostic imaging*
  • Multiple Sclerosis, Relapsing-Remitting / pathology
  • Multiple Sclerosis, Relapsing-Remitting / psychology*
  • Neuropsychological Tests
  • Organ Size

Grants and funding

This work was supported by the National Multiple Sclerosis Society (http://www.nationalmssociety.org/) (RG4463 to AHC, G-1508-08577 to JW); by the Conrad N Hilton Foundation (https://www.hiltonfoundation.org/) (Marilyn Hilton Award for Innovation in MS Research to AHC); the Manny & Rosalyn Rosenthal – Dr. John L. Trotter MS Center Chair in Neuroimmunology of the Foundation for Barnes-Jewish Hospital (https://www.barnesjewish.org/Giving/About-The-Foundation) (AHC).