Longitudinal Persistence of Meningeal Enhancement on Postcontrast 7T 3D-FLAIR MRI in Multiple Sclerosis

S.N. Jonas; I. Izbudak; A.A. Frazier; D.M. Harrison

doi:10.3174/ajnr.A5796

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Fig 1.
Original illustration depicting the 4 morphologies of meningeal enhancement seen in this analysis. Subarachnoid spread/fill pattern (represented by green in A) is an amorphous and ill-defined collection of contrast pooling within the cerebral sulci. The subarachnoid nodular pattern (B) is defined as a punctate, discrete site of meningeal enhancement located within the cerebral sulci abutting the pial surface. The vessel wall pattern (C) is characterized by extension of contrast along the outer margin of large meningeal vessels with a preserved internal flow void creating a characteristic tram-track appearance. The dural pattern (D) is a circumscribed, rounded focus of contrast situated along the dural margin without extension into the subarachnoid space. The perivascular, tubular white structures (seen in schematics A, B, and D) represent the recently discovered meningeal lymphatic system. Reaccumulation of leaked contrast from the CSF into these meningeal lymph channels is a potential mechanism for the venous rim pattern (C).
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Fig 2.
Graph displaying the percentages of baseline enhancing meningeal foci that persist 1 year later (gray bars) and 2 years later (black bars). All 31 participants were scanned at baseline and at 1 year, but 2-year data are limited to 15 participants. At 1 year, persistence was noted in 253/284 (89%) overall foci, 91/114 (80%) subarachnoid spread/fill foci, 10/14 (71%) subarachnoid nodular foci, 104/107 (97%) vessel wall foci, and 46/46 (100%) dural nodular foci. At 2 years, persistence was noted in 132/161 (82%) overall foci, 45/62 (73%) subarachnoid spread/fill foci, 6/7 (86%) subarachnoid nodular foci, 55/55 (100%) vessel wall foci, and 34/34 (100%) dural foci.
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Fig 3.
Examples of persisting foci of meningeal enhancement on delayed postcontrast FLAIR at 7T. Sagittal reformatted images show subarachnoid spread/fill enhancement that persists from December 15, 2015 (A), to March 3, 2017 (B), in a 58-year-old woman with relapsing-remitting MS. Axial images show subarachnoid nodular enhancement that persists from October 8, 2014 (C), to March 3, 2017 (D), in a 49-year-old man with relapsing-remitting MS. Axial images show vessel wall enhancement that persists from March 14, 2016 (E), to April 4, 2017 (F), in a 57-year-old man with primary-progressive MS. Axial images show dural enhancement that persists from May 9, 2016 (G), to May 31, 2017 (H), in a 44-year-old woman with secondary-progressive MS. Note that no intrinsic signal was observed in these locations on precontrast acquisitions (not shown).
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Fig 4.
Examples of resolving foci of meningeal enhancement on delayed postcontrast FLAIR at 7T. Coronal reformatted images show subarachnoid spread/fill enhancement that resolves between October 23, 2014 (A), and February 26, 2016 (B), in a 49-year-old woman with relapsing-remitting MS. Coronal reformatted images show subarachnoid nodular enhancement within the cerebellar folia that resolves between October 8, 2014 (C), and February 19, 2016 (D), in a 49-year-old man with relapsing-remitting MS. Sagittal formatted images show vessel wall enhancement that resolves from May 9, 2016 (E), to May 31, 2017 (F), in a 44-year-old woman with secondary-progressive MS. Note that no foci of meningeal enhancement classified as a dural subtype resolved in this study.

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Table 1:

MRI sequence parameters

Sequence	Resolution (mm)	TR	TI	TE	Parallel Imaging	Flip Angle	Time (min:sec)
MP2RAGE	0.7 × 0.7 × 0.7	TR_volume = 8.25 s	TI₁ = 1 s	1.97 ms	SENSE = 2 × 2	FA₁ = 7°	9:46
		TR_TFE = 6.9 ms	TI₂ = 3.3 s			FA₂ = 5°
MPFLAIR	0.7 × 0.7 × 0.7	8000 ms	2077 ms	400 ms	SENSE = 2 × 3	90°	10:48

Note:—SENSE indicates sensitivity encoding; MPFLAIR, magnetization-prepared FLAIR; FA, flip angle; TFE, turbo field echo.

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Table 2:

Cohort baseline characteristics^{^a}

Characteristics
Age at enrollment (yr)	49 (26–61)
Sex	11/31 Men (35%), 20/31 women (65%)
Disease subtype at enrollment	21/31 (68%) RR, 7/31 (23%) SP,
	3/31 (10%) PP
Disease duration at enrollment (mo)	109 (8–461)
Patients with new relapses in past 30 days	1/31 (3%)
No. of relapses in past year per subject	0 (0–3)
Modified Fatigue Impact Scale score at enrollment	43 (0–78)
Symbol Digit Modality Test at enrollment	50 (35–81)
Expanded Disability Status Scale score at enrollment	3 (1–6.5)
Immunomodulatory treatment status at baseline
On treatment	25/31 (81%)
Not on treatment	6/31 (19%)
Treatment type at baseline
Interferon	3/25 (12%)
Glatiramer	6/25 (24%)
Natalizumab	2/25 (8%)
Teriflunomide	1/25 (4%)
Fingolimod	4/25 (16%)
Dimethyl fumarate	9/25 (36%)
No. of subjects who switched between disease-modifying therapies from baseline to follow-up scans	10/31

Note:—RR indicates relapsing-remitting MS; SP, secondary-progressive MS; PP, primary-progressive MS.
↵a Median values are shown with the range of observed values in parentheses.

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Table 3:

Anatomic distribution within the brain of enhancing meningeal foci at baseline

Brain Region	No. of Foci at Baseline	Percentage of Foci at Baseline
Right frontal	60	21.1
Left frontal	64	22.5
Right parietal	44	15.5
Left parietal	44	15.5
Right occipital	20	7.0
Left occipital	24	8.4
Right temporal	16	5.6
Left temporal	8	2.8
Right cerebellum	2	0.7
Left cerebellum	2	0.7

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Table 4:

Wilcoxon rank sum test for longitudinal persistence of meningeal enhancement versus demographic and clinical factors^{^a}

	On Treatment (n = 25)	Not on Treatment (n = 6)	Progressive MS (n = 10)	Nonprogressive MS (n = 21)	EDSS Progressor at 1 yr^{^b} (n = 7)	EDSS Nonprogressor at 1 yr^{^b} (n = 24)
Total No. of overall foci persisting at 1 yr per subject	9 (1–24)	9 (1–15)	8 (1–24)	9 (1–15)	12 (1–15)	7.5 (1–24)^{^c}
Total No. of subarachnoid spread/fill foci persisting at 1 yr per subject	2 (0–9)	2 (0–6)	2 (0–9)	2 (0–9)	5 (1–9)	2 (0–9)
Total No. of subarachnoid nodular foci persisting at 1 yr per subject	0 (0–2)	0 (0–1)	0 (0–0)	0 (0–2)^{^c}	0 (0–0)	0 (0–2)
Total No. of vessel wall foci persisting at 1 yr per subject	3 (0–11)	3.5 (1–6)	2 (0–6)	3 (0–11)	3 (0–11)	3 (0–7)
Total No. of dural foci persisting at 1 yr per subject	1 (0–9)	1 (0–6)	1 (0–9)	1 (0–6)	1 (0–6)	1 (0–9)

↵a Median values are listed with the range of observed values in parentheses.
↵b Criteria for EDSS progressor status is listed in the “Materials and Methods” section.
↵c P < .05.