Table 2.
Study | Group | Demographics | Clinical variables | MRI | Perfusion assessment approach | Relationship between perfusion metrics and motor assessment | |
---|---|---|---|---|---|---|---|
Assessed relationship | Regions | ||||||
Yin et al., 2018 | RRMS (n = 30) | Age: 13.6 (19–78) 20 females (67%) | EDSS: 1.0 (0.0–5.0) dd: 3.4 (0.2–16.5) | DCE (3T) | ROI-based | Correlation between DCE-derived parameters and EDSS: ○ Non-significant |
Enhancing/non-enhancing WML, NAWM |
Zhang et al., 2018 | RRMS (n =39) | Age: 38.7±12.6 23 females (59%) | EDSS: 2.0 (0.0–6.0) dd: 4.2 ±4.9 | pCASL (3T) | Voxel-wise | Correlation between CBF and EDSS: ○ Positive, significant ○ Negative, significant |
Frontal, temporal, partial parietal, limbic lobes, bilateral putamen, thalamus Occipital, partial frontal, parietal lobes, temporal poles |
HC (n = 73) | Age: 47.7±13.9 55 females (75%) | ||||||
Doche et al., 2017 | RRMS (n = 23) | Age: 34.2±9.3 19 females (83%) | EDSS: 1.5±1.2 MSFC z-score –0.7±1.04 dd: 4.5±4.6 | pCASL (3T) | ROI-based | Correlation between CBF and EDSS: ○ Negative, trend |
Bilateral thalami |
HC (n = 16) | Age: 37.1±10.2 12 females (75%) | Correlation between CBF and MSFC: ○ Positive, significant |
Bilateral thalami | ||||
Correlation between CBF and 9HPT sub-score: ○ Positive, significant |
Bilateral thalami | ||||||
Sowa et al., 2017 | RRMS (early: < 3 years since MS diagnosis) (n = 65) | Age: 34.9±7.2 44 females (66%) | EDSS at follow-up: 2 (1.5–2.5) MSSS at follow-up: 4.2±2.0 | DSC (1.5T) | ROI-based | nCBF: ○ No differences between lower and higher disease severity groups nCBV: ○ No differences between lower and higher disease severity groups nMTT: ○ Lower disease severity group > higher disease severity group |
WML, NAWM WML, NAWM WML, NAWM |
Groups divided based on MSSS at follow-up: | |||||||
Lower disease severity group MSSS≤3.79 | Age: 32.6±6.5 23 females (79%) | dd: 1.9 (1.2–4.0) | |||||
Higher disease severity group MSSS>3.79 (n = 36) | Age: 36.6±6.9 22 females (61%) | 8–2.6) | |||||
Debernard et al., 2014 | RRMS patients (early) (n = 25) | N:25 Age: 37.2±8.6 22 females (88%) | EDSS: 1.5 (0–4.5) MSSS: 3.5±1.8 MSFC: 0.7±0.4 dd: 2.4±1.5 | pCASL (3T) | ○ROI-based ○ Voxel-wise |
Correlation between CBF and EDSS: ○ Non-significant Correlation between CBF and MSFC: ○ Non-significant |
GM GM |
HC (n = 25) | Age: 35.2±10.3 17 females (68%) | Correlation between CBF and MSSS: ○ Non-significant |
GM | ||||
Pailing et al., 2014 | RRMS (n = 35) | Age: 38.1±8.0 23 females (66%) | EDSS: 2.5 (0.0–6.5) dd: 8.2±6.5 | pASL (3T) | ROI-based | Correlation between CBF and EDSS: ○ Non-significant |
NAWM (frontal, occipital, parietal), DGM (thalamus, caudate) |
HC (n = 33) | Age: 40.0±11.1 19 females (58%) | Correlation between BAT and EDSS: ○ Positive, significant (partial, covariates: age, gender, atrophy, WML volume) |
NAWM (frontal, occipital, parietal), DGM (thalamus, caudate) | ||||
Amann et al., 2012 | RRMS (n = 123) | Age: 42.7±10.6 98 females (80%) | EDSS: 2.6±1.3 dd:12.7±8.2 | pCASL (1.5T) | ROI-based | Correlation between CBF and EDSS: ○ Non-significant |
Cortical GM |
SPMS (n = 42) | Age: 54.3±8.3 24 females (57%) | EDSS: 4.6±1.3 dd:12.7±8.2 | |||||
Garaci et al., 2012 | RRMS (n = 33) and SPMS (n = 6) (n = 39) | 26 females (67%), age: 43.1±9.5 13 males (33%), age: 44.9±8.5 | 14 CCSVI-, EDSS: 2.2±1.4 | DSC (3T) | ROI-based | Correlation between CBF and EDSS/MSSS: ○ Non-significant |
NAWM (semioval center, periventricular, frontal, occipital) |
HC (n = 26) | 15 females (58%), age: 40.9±7.2 11 males (42%), age: 40.0±8.2 | 25 CCSVI+, EDSS: 3.0±2.3 | Correlation between CBV and EDSS/MSSS: ○ Non-significant |
NAWM (semioval center, periventricular, frontal, occipital) | |||
Correlation between MTT and EDSS/MSSS: ○ Positive, significant |
NAWM (semioval center, periventricular, frontal, occipital) | ||||||
Inglese et al., 2008 | RRMS (n = 18) | Age: 48 (31–71) 12 females (66.7%) | EDSS: 1 (0–6.5)b dd: 7.6 (1–34)c | DSC (3T) | ROI-based | Correlation between CBF and EDSS: ○ Non-significant. |
DGM (thalamus, putamen, caudate head), NAWM (frontal, periventricular, splenium) |
PPMS (n = 14) | Age: 55 (29–75) 7 females (50.0%) | EDSS: 4 (3–7)b dd: 5 (1–19)c | Correlation between CBV and EDSS: ○ Non-significant |
DGM (thalamus, putamen, caudate head), NAWM (frontal, periventricular, splenium) | |||
HC (n = 11) | Age: 51 (29–65) 7 females (63.6%) | Correlation between MTT and EDSS: ○ Non-significant |
DGM (thalamus, putamen, caudate head), NAWM (frontal, periventricular, splenium) | ||||
Inglese et al., 2007 | RRMS (n = 11) | Age: 46.2 (31–71) 8 females (73%) | EDSS: 1.0 (0.0–6.5) dd: 5.0 (1–13) | DSC (3T) | ROI-based | Correlation between CBF and EDSS: ○ Negative, trend |
DGM (thalamus, putamen, caudate head) |
PPMS (n = 11) | Age: 53.6 (29–71) 4 females (36%) | EDSS: 4.0 (3.0–7.0) dd: 4.0 (1–19) | Correlation between CBV and EDSS: ○ Negative, trend |
DGM (thalamus, putamen, caudate head) | |||
HC (n = 11) | Age: 50.8 (29-65) 7 females (64%) |
Correlation between MTT and EDSS: ○ Non-significant |
DGM (thalamus, putamen, caudate head) | ||||
Adhja et al. 2006 | RRMS (n = 11) | Age: 46.2 (31–71) 8 females (73%) | EDSS: 1.0 (0.0– 6.5) dd: 5 (1–13) | DSC (3T) | ROI-based | Correlation between CBF and EDSS: ○ Negative, significant |
NAWM (periventrivular) |
PPMS (n = 11) | Age: 53.6 (29–71) 4 females (36%) | EDSS: 4.0 (3.0–7.0) dd: 4 (1–19) | Correlation between CBV and EDSS: ○ Negative, significant |
NAWM (frontal, periventrivular) | |||
HC (n = 11) | Age: 50.8 (29–65) 7 females (64%) | Correlation between MTT and EDSS: ○ Non-significant | NAWM (frontal, periventrivular, splenium, occipital) | ||||
Rashid et al., 2004 | RRMS (n = 21) | Age: 38.9 (17–59) 13 females (62%) | EDSS: 2.5 (0–6.5) dd: 10 (1–31) | CASL (1.5T) | ROI-based Voxel-wise | Correlation between CBF and EDSS: ○ Non-significant | WM, whole brain |
SPMS (n = 14) | Age: 51.2 (30–65) 11 females (79%) | EDSS: 6.0 (2–8) dd: 18 (7–40) | Correlation between CBF and MSFC: ○ Non-significant | WM, whole brain | |||
PPMS (n = 12) | Age: 55.7 (40–69) 7 females (58%) | EDSS: 6.5 (3.5–8.5) dd: 16 (8–34) | |||||
Benign MS (n = 13) | Age: 52.6 (40–60) 8 females (62%) | EDSS: 2.5 (1–3) dd: 24 (20–36) | |||||
HC (n = 34) | Age: 40.7 (20–67) 19 females (56%) |
Age and dd are reported in years. Values are provided as mean ± standard deviation or median (range). The percentage of females out of the total number of subjects is expressed in parenthesis after the female number. CCSVI: Chromic cerabrospinal venous insufficiency; ASL: arterial spin labeling; CBF: cerebral blood flow; BAT: Bolus Arrival Time; CBV: cerebral blood volume; dd: disease duration; CASL: Continuous Arterial Spin Labeling; DGM: deep gray matter; DCE: Dynamic Contrast-Enhanced; DSC: Dynamic Susceptibility Contrast; EDSS: Expanded Disability Status Scale; HC: healthy controls; GM: gray matter; L: left; MS: multiple sclerosis; MSFC: Multiple Sclerosis Functional Composite Measure (including leg function evaluated by the timed 25-foot walk (25FTW), nine-hole peg test (9HPT), and three-second paced auditory serial addition test (PASAT3)); MSSS: Multiple Sclerosis Severity Score; MTT: mean transit time; NAGM–normal appearing gray matter; NAWM: normal-appearing white matter; nCBF: average CBF in the whole WML divided by CBF in NAWM; nCBV: average CBV in the whole WML divided by CBF in NAWM; nMTT: average MTT in the whole WML divided by CBF in NAWM; PASAT: Paced Auditory Serial Addition Test; PPMS: primary progressive multiple sclerosis; pCASL: pseudo Continuous Arterial Spin Labeling; R: right; ROI: region of interest; RRMS: relapsing-remitting multiple sclerosis; WM: white matter; WML: white matter lesions; SPMS: secondary progressive multiple sclerosis.