Muscle MRI in motor neuron diseases: a systematic review

Figures & data

Figure 1 PRISMA flow diagram of the study appraisal process.

Table 1 Studies included in a literature review.

Paper	Outline	Participants	Clinical Measurements	MRI Measurements
MND
Cha and Patten (18)	Investigates tongue morphological and microarchitectural changes in ALS	16 ALS 20 other-disease	Dynamometry (grip strength)	Volume (quantitative) Internal structure (qualitative)
Bryan et al. (19)	Characterises leg muscle abnormalities and correlations with standard neurological clinical tests in ALS patients measured at 0 and 4 months	11 ALS 8 HCs	CMAP, MVIC and NCS.	Volume and T1/T2 relaxation time (quantitative)
Jenkins et al. (24)	Measures muscle volume changes in ALS patients and controls over 12 months	6 ALS 14 HCs	MVIC, dynamometry, MUNE	Volume (quantitative)
Staff et al. (25)	Assesses MRI abnormalities of peripheral nerves and muscle in ALS and MMN	60 ALS 8 MMN	Muscle strength testing scored with neuropathy impairment score	Visual abnormality score (qualitative)
Gerevini et al. (26)	Assesses MRI of the brachial plexus and limb girdle muscles in ALS	23 ALS 12 HCs	MRC, UMN burden score, ALSFRSr	Signal intensity alterations, edema, Stramare score, and Mercuri score (all qualitative)
Jenkins et al. (27)	Assesses clinical, electrophysiological, and whole-body muscle MRI measurements of progression in MND at 0 and 4 months	26 ALS, 3 PMA 22 HCs	ALSFRSr, MRC, Handheld dynamometry, Maximal CMAP, MUNIX	Relative T2 signal (semi-quantitative)
Lee et al. (23)	Assesses differences in tongue microarchitecture between ALS patients and controls.	2 ALS 5 HC	ALSFRSr	Mean diffusivity and fractional anisotropy (quantitative)
Diamanti et al. (28)	Images of hand, paraspinal and lower limb muscles in newly diagnosed ALS patients are compared against clinical findings and controls	10 ALS 9 HC	ALSFRSr and UMN burden score MUAPs MRC	Mercuri scale (qualitative)
Kronlage et al. (21)	Magnetic resonance neurography used to assess fascicular lesions and muscle denervation signs for differentiation between ALS and MMN.	22 ALS 8 MMN 15 HCs	–	Visual muscle denervation score (qualitative)
Diamanti et al. (30)	Evaluates the role of paraspinal muscle MRI as a diagnostic biomarker in ALS	14 ALS 11 HCs 10 inflammatory myopathy 19 lumbar radiculopathy	ALSFRSr	Mercuri scale (qualitative)
Jenkins et al. (31)	Measures longitudinal changes in clinical, electrophysiological and MRI data measured at 0, 4 and 12 months in MND patients	26 ALS, 3 PMA 22 HCs	ALSFRSr, MRC, Handheld dynamometry, CMAP, MUNIX, MUSIX	Relative T2 signal (semiquantitative) Apparent diffusion coefficient (quantitative)
Hensiek et al. (22)	Assesses tongue muscle volume and T1 intensity in a cohort of ALS and PLS patients	175 ALS 10 PLS 104 HCs	ALSFRSr Ventilation status Gastrostomy status	Volume and mean T1 signal intensity (quantitative)
SMA
Liu et al. (41)	Describes muscle MRI findings of the lower extremity in SMA	17 SMA	–	Visual grading of fat infiltration and atrophy (qualitative)
Mercuri et al. (36)	Thigh muscle MRI is performed on SMA patients with a rare phenotype	11 SMA	EMG, muscle biopsy, ECG, FVC, muscle power, functional ability	Mercuri scale (qualitative)
Sproule, Punyanitya, et al. (32)	Compares muscle volume and signal against dual-energy X-ray absorptiometry and clinical measurements in SMA	14 SMA	Dual-energy X-ray absorptiometry, HFMSE, Handheld dynamometry, CMAP, MUNE	Volume (quantitative) Binarised into normal or abnormal signal (qualitative)
Sproule, Montgomery, et al. (33)	Investigates 6-month changes in thigh muscle volume in SMA	11 SMA	HFMSE	Volume (quantitative) Binarised into normal or abnormal signal (qualitative)
Durmus et al. (37)	Describes the pattern of muscle involvement in SMA type IIIb	25 SMA	MRC	Fischer scale (qualitative)
Bonati et al. (35)	four muscle MRI scans were performed over 1 year to assess changes in quantitative MRI measurements	18 SMA 19 HC	Motor function measure score 6MWT	Fat fraction, cross-sectional area, water-T2 signal (all quantitative)
Kollmer et al. (38)	Describes MR neurography of lesions in SMA, compares findings against clinical measurements	31 SMA 31 HCs	ALSFRSr, CMAP, Sensory nerve action potentials and NCS, HFMSE, Revised Upper Limb Module, 6MWTD.	Modified Goutallier classification (qualitative)
Brogna et al., (40)	Describes pattern of muscle involvement in patients with types 2 and 3 SMA	55 SMA	HFMSE	Mercuri scale (qualitative)
Barp et al. (39)	Two year follow up involving muscle MRI of two SMA patients after taking nusinersen	2 SMA	Revised upper limb module and HFMSE	Mercuri scale (qualitative) Tractography and fractional anisotropy (quantitative)
Otto et al. (42)	Describes muscle involvement patterns in the lower limbs of types II and III SMA patients using quantitative MRI	31 SMA 20 HC	HFMSE MRC	Fat fraction, water-T2 signal, mean diffusivity, fractional anisotropy (all quantitative)
Otto et al. (43)	Measures longitudinal changes in quantitative MRI results from the lower limbs of types II and III SMA patients	10 SMA	HFMSE MRC dynamometry	Fat fraction, water-T2 signal, mean diffusivity, fractional anisotropy (all quantitative)
Savini et al. (44)	Muscle fat fraction and T2 signal assessed every 4 months for 21 months in a cohort of SMA IIIa patients on nusinersen	3 SMA 11 HC	Neurological examination, HFMSE, RULM, 6MWT	Fat fraction, water-T2 signal (quantitative)
Souza et al. (34)	Assesses clinical and radiological features of a cohort of SMA IV patients	20 SMA 15 HC 15 other-SMA phenotype controls	HFMSE, ALSFRSr, RULM, SMAFRS, fatigue severity score, 6MWT, time up and go test, MRC, NCS, EMG, MUNIX	Mercuri scale (qualitative)
SBMA
Hamano et al. (20)	Investigates the pattern of muscle involvement in SBMA	3 SBMA 2 ALS 1 HC	–	Visual assessment of signal intensity and muscle atrophy (qualitative)
Klickovic et al. (29)	Qualitative MRI and clinical measurements compared between ALS and SBMA cohorts	21 SBMA 21 ALS 16 HCs	ALSFRSr SBMAFRS Adult myopathy assessment tool	Mercuri scale (qualitative) Morrow scale (qualitative) Fat fraction & cross-sectional area (quantitative)
Dahlqvist et al. (45)	Observational cross-sectional study. MRI used to describe muscle degeneration in SBMA and findings are correlated with clinical measures	40 SBMA 25 HCs	Dynamometry. 6MWTD. SBMAFRS and bulbar rating scale. Swallowing function. BMI. Total body fat with dual-energy X-ray absorptiometry. ECG. FVC. blood biochemistry and sex hormones.	Mercuri scale (qualitative) Fat fraction & cross-sectional area (quantitative)

6MWTD: 6 minute walk test distance; ALSFRSr: ALS functional rating scale revised; BMI: body mass index; CMAP: compound muscle action potential; DTI: diffusion tensor imaging; DWI: diffusion weighted imaging; ECG: electrocardiogram; EMG: electromyography; FVC: forced vital capacity; HC: healthy control; HFMSE: Hammersmith functional motor scale expanded; MMN: multifocal motor neuropathy; MRC: medical research council (muscle strength scale); MUNE: motor unit number estimation; MUNIX: motor unit number index; MUSIX: motor unit size index; MVIC: maximum voluntary isometric contraction; NCS: nerve conduction studies; PLS: primary lateral sclerosis; PMA: primary muscular atrophy; SBMA: spinal bulbar muscular atrophy; SBMAFRS: SBMA functional rating scale; SMAFRS: SMA functional rating scale; TA: tibialis anterior.

Table 2 MRI acquisition sequences.

Paper	Sequence	Field strength (T)	Slice thickness (mm)	Matrix size	Repetition time (msec)	Echo time (msec)	Plane	Field of view (mm)	Scan time (min:sec)
MND
Cha and Patten (18)	T1 SE	0.5/1	5–6	256 × 256	50–600	15–35	Sag	–	–
Bryan et al. (19)	T1 & T2 3D vol grad echo	–	1.6	205 × 256	2000	20–160	Cor/ax	450	–
Jenkins et al. (24)	3D T1 FFE	3.0	1	–	25	3.5	Ax/sag	–	–
	T2 TSE	3.0	6	–	2600	100	Cor	–	–
	3D T1 FFE	3.0	1.6	–	11	4.8	Sag	–	–
Gerevini et al. (26)	PD FSE	1.5	3	292 × 224	3500	30		307 × 307	40:00
	T2 FSE	1.5	3	456 × 360	6038	100	Cor	307 × 307
	3D T2 FSE	1.5	3	252×250×360	2250	230	Sag/cor	250×250×180
	STIR	1.5	3	376 × 300	4086	60	Cor	307 × 307
	T1 FSE	1.5	3	384 × 308	543	18	cor	307 × 307
	3D T1 FFE	1.5	3	356 × 543 × 94	24	4.6	Ax	349 × 349 × 160
Jenkins et al. (27)	T2 FSE	3	5	–	1107	80	Cor	–	–
Lee et al. (23)	T2 TSE	3	1.2	256 × 256 × 200	3380	107	Sag	–	–
	DWI SSSE EPI	–	4.6	128x128x72	2300	55	Sag	–	–
Diamanti et al. (28)	T1	1.5	10	–	500	15	Ax/sag	–	–
	T1	1.5	10	–	500	8	Ax	–	–
	T1	1.5	3	–	300	10	Ax/cor	–	–
Kronlage et al. (21)	2D T2 TSE	3.0	3.5	512 × 333	8150	54	Ax	160 × 160	–
	3D T2 SPACE	3.0	1	320 × 320	3000	206	Cor/Ax	305 × 305	–
Diamanti et al. (30)	T1 TSE	3.0	10	512 × 512	803	11	Ax	230	–
	T1 TSE	3.0	5	512 × 512	714	12	Cor	400	–
Jenkins et al. (31)	T2 FSE	3.0	5	–	1107	80	Cor	–	20:00
	DWI	3.0	5	–	9412	66	Ax	–	40:00
Hensiek et al. (22)	3D T1 MPRAGE	3.0	1	256x256x192	2500	4.82	Sag	–
SMA
Liu et al. (41)	T1 SE	0.5	–	–	600	20	Ax/Cor	–	15:00
Mercuri et al. (36)	T1 SE	1.0	5	256 × 256	500	20	Ax	250-500	–
Sproule et al. (32,33)	T1 FSE	1.5	5	–	–	–	–	–	30:00
Durmus et al. (37)	T1 TSE	1.5	5	384 × 384	561	14	Ax	440 × 400	2:22
	T2 TSE	1.5	3	272z224	4135	120	Ax	340 × 340
	T1 TSE	1.5	5.5	320 × 320	480	12	Ax	230 × 230	2:06
	T2 TSE	1.5	4	384 × 384	5700	128	Ax	170 × 170	2:13
Bonati et al. (35)	T2 SE	3.0	3	384 × 384	1800	9.1 − 127.4	–	400 × 400
	3D VIBE	3.0	3	384 × 384	20	2.46, 3.96	–	400 × 400
	6-echo 3D VIBE	3.0	3	384 × 384	20	1.53 − 8.33	–	400 × 400
Kollmer et al. (38)	3D T2 IR SPACE	3.0	1	320x320x104	3000	205	Ax	305 × 305	12:17
	2D TSE	3.0	3.5	512 × 512	5860	14-86	Ax	170 × 170	33:40
Brogna et al., 2020	T1 FSE	–	5	–	550	8	Ax	–	20
Barp et al. (39)	T1	1.5	10	–	530	9.9	Ax	–	–
	STIR	1.5	10	–	4000	94	Ax	–	–
	MSE	1.5	4	124 × 123	2860	10-100	Ax	160 × 160	–
	DTI	1.5	4	–	7500	71	Ax	250 × 72.5	–
Otto et al. (42),	4-point Dixon	3.0	6	320 × 320	210	2.6/3.4/4.1/4.9	–	480 × 480	1:20
	T2 MSE	3.0	6	–	4598	17 × 7.6	–	–	3:05
	DWI SE EPI	3.0	6	160 × 92	5000	57	–	480 × 276	3.30
Savini et al. (44)	3D 6-point GRE	3.0	5	432 × 396 × 52	35	1.7–9.2	–	–	15
	T2 TSE	3.0	10	–	4100	10.9	–	–
Souza et al. (34)	T1 SE	1.5	7	360–464 × 512	335	19	Ax	–	–
	STIR	1.5	7	480–576 × 512	3650	52	Ax	–	–
SBMA
Hamano et al. (20)	T1	1.0–1.5	–	–	333–516	14–10.7	–	–	–
Klickovic et al. (29)	3-point Dixon, T1, STIR	3.0	–	–	–	–	–	–	35:00
Dahlqvist et al. (45)	T1	3.0	6	–	450	21	–	170	–
	T1	3.0	6	–	650	19	–	400–450	–
	2-point Dixon	3.0	3.5	–	3.675/5.59	2.45	–	400–450	–
	T1	3.0	3	–	656	39	–	200	–
	2-point Dixon	3.0	2	–	3.675/5.64	2.45	–	245	–

Cells marked ‘-‘indicate data not provided by the author. Ax: axial; Cor: coronal; DTI: diffusion tensor imaging; GRE: gradient echo; IR: inversion recovery; SE: spin echo; SSSE: single-shot spin-echo; EPI: echo-planar imaging; MPRAGE: magnetization prepared rapid gradient echo; MSE: multi-echo spin-echo; Sag: sagittal; SPACE: sampling perfection with application-optimised contrasts using different flip angle evolution; STIR: short-tau inversion recovery; VIBE: volumetric interpolated breath-hold examination.

Table 3 Assessment of bias using the NHLBI quality assessment tool.

	Cha and Patten (18)	Bryan et al. (19)	Jenkins et al. (24)	Staff et al. (25)	Gerevini et al. (26)	Jenkins et al. (27)	Lee et al. (23)
Research objective clearly stated?	✓	✓	✓	✓	✓	✓	✓
Study population clearly defined?	✕	✓	✓	✓	✓	✓	✕
Subjects recruited from similar populations with uniform entry criteria?	✕	✓	✓	✓	✓	✓	✕
Sample size justification, power description, or variance and effect estimates provided?	✕	✕	✕	✕	✕	✓	✕
Were the exposures of interest measured prior to the outcomes being measured?	✓	✓	✓	✓	✓	✓	✓
Sufficient timeframe allowed for association between exposure and outcome?	✕	✕	✓	✕	✕	✕	✕
Were the exposure measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✕	✓	✓	✕
Were the outcome measures clearly defined, valid, reliable, and implemented consistently?	✕	✓	✓	✓	✓	✓	✓
Were the outcome assessors blinded to the exposure status of participants?	✕	✕	✓	✓	✓	✓	✕
Was loss to follow-up after baseline 20% or less?	–	✕	✕	–	–	✕	–
Were key potential confounding variables measured and adjusted?	✕	✕	✕	✕	✕	✓	✕
NOS score	1/8	3/9	5/9	2/8	6/8	7/9	0/8
	Diamanti et al. (28)	Kronlage et al. (21)	Diamanti et al. (30)	Jenkins et al. (31)	Hensiek et al. (22)	Liu et al. (41)	Mercuri et al. (36)
Research objective clearly stated?	✓	✓	✓	✓	✓	✓	✓
Study population clearly defined?	✓	✓	✓	✓	✓	✕	✓
Subjects recruited from similar populations with uniform entry criteria?	✓	✓	✓	✓	✓	✕	✕
Sample size justification, power description, or variance and effect estimates provided?	✕	✕	✕	✓	✓	✕	✕
Were the exposures of interest measured prior to the outcomes being measured?	✓	✓	✓	✓	✓	✓	✓
Sufficient timeframe allowed for the association between exposure and outcome?	✕	✕	✕	✓	✕	✕	✕
Were the exposure measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✓	✓	✓	✓
Were the outcome measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✓	✓	✕	✓
Were the outcome assessors blinded to the exposure status of participants?	✓	✓	✓	✕	✓	✕	✕
Was the loss to follow-up after baseline 20% or less?	–	–	–	✕	–	–	–
Were key potential confounding variables measured and adjusted?	✕	✕	✕	✕	✕	✕	✕
NOS score	6/8	7/8	6/8	5/9	8/8	2/8	2/8
	Sproule, Punyanitya, et al. (32)	Sproule, Montgomery, et al. (33)	Durmus et al. (37)	Bonati et al. (35)	Kollmer et al. (38)	Brogna et al. (40)	Barp et al. (39)
Research objective clearly stated?	✓	✓	✓	✓	✓	✓	✓
Study population clearly defined?	✕	✕	✓	✓	✓	✓	✓
Subjects recruited from similar populations with uniform entry criteria?	✕	✕	✕	✓	✓	✓	✕
Sample size justification, power description, or variance and effect estimates provided?	✕	✕	✕	✕	✓	✕	✕
Were the exposures of interest measured prior to the outcomes being measured?	✓	✓	✓	✓	✓	✓	✓
Sufficient timeframe allowed for the association between exposure and outcome?	✕	✕	✕	✕	✕	✕	✓
Were the exposure measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✓	✓	✕	✓
Were the outcome measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✓	✓	✓	✓
Were the outcome assessors blinded to the exposure status of participants?	✓	✓	✓	✕	✓	✕	✕
Was the loss to follow-up after baseline 20% or less?	–	✓	–	✓	–	–	✓
Were key potential confounding variables measured and adjusted?	✓	✓	✕	✓	✕	✕	✕
NOS score	4/8	4/9	5/8	7/9	8/8	2/8	4/9
	Otto et al. (42)	Otto et al. (43)	Savini et al. (44)	Souza et al. (34)	Hamano et al. (20)	Klickovic et al. (29)	Dahlqvist et al. (45)
Research objective clearly stated?	✓	✓	✓	✓	✕	✓	✓
Study population clearly defined?	✓	✓	✕	✓	✕	✓	✓
Subjects recruited from similar populations with uniform entry criteria?	✓	✓	✕	✓	✕	✓	✕
Sample size justification, power description, or variance and effect estimates provided?	✕	✕	✕	✕	✕	✕	✕
Were the exposures of interest measured prior to the outcomes being measured?	✓	✓	✓	✓	✓	✓	✓
Sufficient timeframe allowed for the association between exposure and outcome?	✕	✓	✓	✕	✕	✕	✕
Were the exposure measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✓	✓	✓	✓
Were the outcome measures clearly defined, valid, reliable, and implemented consistently?	✓	✓	✓	✓	✕	✓	✓
Were the outcome assessors blinded to the exposure status of participants?	✕	✕	✓	✕	✕	✓	✕
Was the loss to follow-up after baseline 20% or less?	–	✕	✓	–	–	–	–
Were key potential confounding variables measured and adjusted?	✓	✕	✕	✕	✕	✕	✕
NOS score	6/8	3/9	7/9	6/8	2/8	7/8	6/8

Table 4 Assessment of bias in cohort studies using the NOS.

	Bryan et al. (19)	Jenkins et al. (24)	Jenkins et al. (27)	Jenkins et al. (31)	Sproule, Montgomery, et al. (33)	Bonati et al. (35)	Barp et al. (39)	Savini et al. (44)	Otto et al. (43)
Representativeness of the exposed cohort	*	*	*	*		*
Selection of the non-exposed cohort			*	*
Ascertainment of exposure	*	*	*	*	*	*	*	*	*
Demonstration that outcome not present at the start of the study	*	*	*	*	*	*	*	*	*
Comparability of cohorts on the basis of design or analysis			**			**		**
Assessment of outcome		*	*		*			*
Was follow-up long enough		*		*		*	*	*	*
Adequacy of follow-up of cohorts					*	*	*	*
Total score	3/9	5/9	7/9	5/9	4/9	7/9	4/9	7/9	3/9

Table 5 assessment of bias in cross-sectional studies using the NOS.

	Cha and Patten (18)	Staff et al. (25)	Gerevini et al. (26)	Lee et al. (23)	Diamanti et al. (28)	Kronlage et al. (21)	Diamanti et al. (30)	Hensiek et al. (22)	Liu et al. (41)	Mercuri et al. (36)
Representativeness of the sample		*	*		*	*	*	*		*
Sample size justification								*
Ascertainment of exposure	*		**		**	**	**	**	**	*
Comparability of cohorts on the basis of design or analysis			*		*	**	*	**
Assessment of outcome		*	*		*	*	*	*
Statistical test			*		*	*	*	*
Total score	1/8	2/8	6/8	0/8	6/8	7/8	6/8	8/8	2/8	2/8
	Sproule, Punyanitya, et al. (32)	Durmus et al. (37)	Kollmer et al. (38)	Otto et al. (42)	Brogna et al. (40)	Souza et al. (34)	Hamano et al. (20)	Klickovic et al. (29)	Dahlqvist et al. (45)
Representativeness of the sample		*	*	*	*	*		*	*
Sample size justification			*
Ascertainment of exposure	**	**	**	**		**	**	**	**
Comparability of cohorts on the basis of design or analysis			**	**		**		**	**
Assessment of outcome	*	*	*					*
Statistical test	*	*	*	*	*	*		*	*
Total score	4/8	5/8	8/8	6/8	2/8	6/8	2/8	7/8	6/8

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