Magnetic resonance imaging derived biomarkers for the diagnosis of type 2 diabetes with insulin resistance: A pilot study

Table 1 Parameters of magnetic resonance imaging study protocols

Sequence	T1WI	T2WI	FS-T2WI	Q-Dixon	DTI
Orientations	Sagittal	Sagittal	Sagittal	Axial	Axial
TR (ms)	500	2780	2360	10.02	4950
TE (ms)	9.3	83	41	1.45	75
Resolution (mm3)	0.8 × 0.8 × 4	0.8 × 0.8 × 4	0.8 × 0.8 × 4	1.2 × 1.2 × 3.5	1.25 × 1.25 × 5
Echo number	1	1	1	1	1
Number of averages	1	1	3	1	1
Echo train length	3	19	11	6	0
Slice thickness (mm)	4	4	4	3.5	5
FOV (mm2)	359 × 359	359 × 359	359 × 359	393 × 450	1015 × 1680
FA (°)	150	160	128	4	180
BW (Hz/px)	285	250	445	1085	850

TR: Repetition time; TE: Echo time; FOV: Field of view; FA: Flip angle; BW: Bandwidth; T1WI: T1-weighted imaging; T2WI: T2-weighted imaging; Q-Dixon: Quantitative Dixon; DTI: Diffusion tensor imaging.

Table 2 Basic characteristics of subjects, mean ± SD/n (total)

Parameters	Control	T2DM-nonIR	T2DM-IR	P value
Basic characteristics
Age (years)	55.31 ± 9.55	55.40 ± 7.97	61.67 ± 8.93	0.031
Sex	F: 27, M: 11	F: 23, M: 17	F: 8, M: 10	0.145
Height (m)	1.64 ± 0.05	1.62 ± 0.08	1.61 ± 0.08	0.151
Weight (kg)	64.65 ± 9.10	62.57 ± 9.07	64.36 ± 9.72	0.742
BMI (kg/m2)	23.83 ± 2.97	23.76 ± 2.55	24.91 ± 2.82	0.395
Waist circumstance (cm)	78.63 ± 24.07	87.57 ± 10.59	93.67 ± 7.45	0.021
Diabetes history
Disease course (years)	/	6.93 ± 6.68	11.94 ± 8.92	0.000
Bad control of diabetes	0 (39)	35 (40)	15 (18)	0.000
Blood glucose (mmol/L)	4.88 ± 0.20	13.10 ± 7.47	10.93 ± 5.47	0.011
HbA1c (%)	/	8.59 ± 2.77	8.20 ± 1.60	0.911
HOMA-IR	/	0.66 ± 0.37	4.48 ± 3.02	0.000
Insulin (μIU/mL)	/	19.38 ± 12.39	44.55 ± 38.30	0.087
C-peptide (ng/mL)	/	3.89 ± 2.32	4.09 ± 3.02	0.874
Cardiovascular history and dyslipidemia
Cardiovascular disease	0	1	2	0.088
Hypertension	11 (39)	15 (40)	7 (18)	0.609
Total cholesterol	/	4.20 ± 0.97	3.95 ± 1.11	0.495
Triglyceride	/	1.89 ± 1.31	1.68 ± 1.13	0.296
HDL-C	/	1.09 ± 0.23	1.20 ± 0.45	0.545
Lifestyle
Smoking history	1 (39)	6 (40)	3 (18)	0.081
Alcohol history	1 (39)	7 (40)	3 (18)	0.050

T2DM-nonIR: Type 2 diabetes mellitus without insulin resistance; T2DM-IR: Type 2 diabetes mellitus with insulin resistance; BMI: Body mass index; HbA1c: Glycated hemoglobin; HOMA-IR: Homeostatic Model Assessment of insulin resistance; HDL-C: High-density lipoprotein cholesterol.

Table 3 Multiparametric magnetic resonance imaging quantification of muscles and vertebrae, mean ± SD

	Parameters	Control	T2DM-nonIR	T2DM-IR	P value
Psoas	FF (‰)	84.39 ± 28.82	83.34 ± 32.95	87.55 ± 22.52	0.449
	Total fat content	16.01 ± 6.87	13.72 ± 5.34	21.35 ± 7.07	0.003
	IMCL	8.24 ± 5.85	6.64 ± 4.60	14.63 ± 8.24	0.001
	EMCL	7.77 ± 2.23	7.08 ± 1.89	6.73 ± 3.50	0.564
	CSA	3.88 ± 1.05	3.82 ± 1.14	2.96 ± 0.91	0.047
	FA	0.63 ± 0.04	0.59 ± 0.04	0.56 ± 0.10	0.040
	ADC (10-3)	1.92 ± 0.36	2.23 ± 0.84	1.89 ± 0.15	0.027
	FMR	16.76 ± 7.22	21.04 ± 10.76	20.22 ± 7.22	0.046
	IMCL/M	54.38 ± 129.36	62.55 ± 84.18	101.06 ± 147.59	0.005
	EMCL/M	40.86 ± 17.64	38.17 ± 15.42	47.21 ± 88.11	0.159
Erector	FF (‰)	112.74 ± 56.49	100.30 ± 40.80	108.23 ± 46.64	0.964
	Total fat content	11.01 ± 4.23	9.66 ± 3.99	13.48 ± 3.24	0.005
	IMCL	4.27 ± 2.66	3.40 ± 2.25	6.14 ± 2.84	0.004
	EMCL	6.74 ± 1.98	6.26 ± 2.25	7.34 ± 1.81	0.216
	CSA	10.60 ± 3.00	9.95 ± 2.09	9.11 ± 2.55	0.042
	FA	0.54 ± 0.05	0.52 ± 0.08	0.56 ± 0.06	0.164
	ADC (10-3)	1.98 ± 0.17	2.12 ± 0.78	2.01 ± 0.15	0.631
	FMR	81.59 ± 41.48	113.81 ± 83.39	71.12 ± 25.22	0.224
	IMCL/M	185.40 ± 103.40	261.12 ± 224.05	666.34 ± 971.10	0.040
	EMCL/M	126.47 ± 55.13	160.31 ± 91.44	130.31 ± 42.99	0.314
Multifidus	FF (‰)	121.86 ± 54.53	114.83 ± 37.99	115.42 ± 43.86	0.846
	Total fat content	41.42 ± 22.49	41.12 ± 19.27	52.70 ± 16.48	0.040
	IMCL	32.47 ± 20.38	32.90 ± 16.88	40.54 ± 122.43	0.093
	EMCL	9.95 ± 4.92	8.22 ± 3.97	12.17 ± 9.24	0.216
	CSA	2.03 ± 0.63	1.912.03 ± 0.45	3.24 ± 0.48	0.450
	FA	0.55 ± 0.05	0.51 ± 0.06	0.55 ± 0.06	0.061
	ADC (10-3)	2.02 ± 0.14	2.01 ± 0.23	2.01 ± 0.18	0.639
	FMR	4.14 ± 1.73	4.99 ± 3.46	5.48 ± 7.74	0.513
	IMCL/M	5.72 ± 3.20	7.41 ± 7.31	6.97 ± 8.68	0.858
	EMCL/M	32.64 ± 54.53	24.23 ± 12.64	61.38 ± 107.41	0.353
L4 vertebra	R2*	145.84 ± 58.01	142.33 ± 44.93	129.65 ± 43.47	0.631
	T2*	90.97 ± 89.30	91.08 ± 88.21	96.35 ± 93.89	0.248
	FF (‰)	518.33 ± 106.84	519.13 ± 128.53	554.33 ± 125.92	0.285
L5 vertebra	R2*	149.45 ± 64.30	143.26 ± 46.26	134.87 ± 37.74	0.526
	T2*	82.06 ± 43.06	80.61 ± 57.181	95.60 ± 186.02	0.216
	FF (‰)	517.97 ± 107.90	521.58 ± 140.35	584.97 ± 104.66	0.043

T2DM-nonIR: Type 2 diabetes mellitus without insulin resistance; T2DM-IR: Type 2 diabetes mellitus with insulin resistance; FF: Fat fraction; IMCL: Intramyocellular lipid; EMCL: Extramyocellular lipid; CSA: Cross-sectional area; FA: Fractional Anisotropy; ADC: Apparent diffusion coefficient; FMR: Fat-muscle ratio; IMCL/M: Intramyocellular lipid/muscle ratio; EMCL/M: Extramyocellular lipid/muscle.

Table 4 Receiver operating characteristic curve parameters for the diagnosis of type 2 diabetes mellitus with insulin resistance

Feature	AUC	Sensitivity	Specificity
E IMCL	0.838	0.800	0.938
E IMCL/M	0.562	0.800	0.500
E total fat content	0.812	0.800	0.813
P FMR	0.650	0.600	0.875
P IMCL/M	0.688	0.800	0.625

E: Erector; P: Psoas; IMCL: Intramyocellular lipid; IMCL/M: Intramyocellular lipid/muscle ratio; FMR: Fat-muscle ratio; AUC: Area under the curve.

Table 5 Receiver operating characteristic curve parameters of the diagnosis of type 2 diabetes mellitus-insulin resistance with magnetic resonance imaging biomarkers and clinical factors

Feature	AUC	Sensitivity	Specificity
E IMCL	0.887	0.800	0.938
E IMCL/M	0.825	0.725	0.688
E total fat content	0.875	0.775	0.625
P FMR	0.738	0.600	0.938
P IMCL/M	0.775	0.800	0.667

E: Erector; P: Psoas; IMCL: Intramyocellular lipid; IMCL/M: Intramyocellular lipid/muscle ratio; FMR: Fat-muscle ratio; AUC: Area under the curve.