How to select the quantitative magnetic resonance technique for subjects with fatty liver: A systematic review

Table 1 Studies reporting on the measurement of the hepatic fat content with ¹H-magnetic resonance spectroscopy versus liver biopsy and other imaging methods

Ref.	Year	Study design	Age (year)	N	Etiology	Field strength sequence	Comparison	Interval	Results
Thomsen et al[22]	1994		48	14	Fatty liver	1.5 T. STEAM (TE = 34 ms)	Liver biopsy		r = 0.897; P < 0.001
Longo et al[26]	1995		45	29	Diffuse steatosis	1.5 T. PRESS (TE = 50–200 ms)	Liver biopsy		r = 0.70
Cowin et al[30]	2008		42	12	Steatosis	1.5 T. PRESS (TE = 30 ms)	Liver biopsy	6 wk	r = 0.928; P < 0.0001
Irwan et al[63]	2008	Prospective	47	10	Healthy volunteers	1.5 T. PRESS (TE = 30 ms)	Dual-echo imaging	One measurement session	r = 0.927. In the range 1%–10%, the MRI-determined the liver fat contents (corrected algorithm) are systematically higher, on average 4% (range: 2.1%–6.1%) than those obtained with MRS
Kim et al[64]	2008	Prospective	15.9 ± 5.3	28	Lean and obese	1.5 TPRESS (TE = 20 ms)	Two-Point Dixon		r = 0.954; P < 0.001
Borra et al[65]	2009	Prospective	62.8 ± 8.3	33	Type 2 diabetes	1.5 T. PRESS (TE = 25 ms)	IP/OP (Dixon)		r = 0.959–0.962; P < 0.001
Reeder et al[66]	2009	Prospective	49.0 ± 12	31	Suspected steatosis and unrelated reasons	1.5 T. PRESS (TE = 25 ms)	IDEAL		r = 0.83 ± 0.05; P < 0.001. Intercept (1.76 ± 0.76%; P = 0.03)
Zhong et al[31]	2009		50 ± 12	36	Fatty liver	3.0 T. PRESS (TE = 144 ms)	16-row multislice CT		r = –0.461; P = 0.005
Hu et al[67]	2010			16		3.0 T. PRESS (TE = 23 ms)	IDEAL		Slope = 0.90, intercept = 1.07%; r2 = 0.95, P < 0.001
Roldan-Valadez et al[68]	2010		35	18	Steatosis	3.0 T	Liver biopsy		r = 0.876; P ≤ 0.001
Mehta et al[32]	2010		39.9	50	Steatosis	1.5 T. PRESS (TE = 135 ms)	Ultrasound		BMI > 30, sensitivity 96%; BMI ≤ 30, sensitivity 64%
Meisamy et al[23]	2011	Prospective	40	55		1.5 T. STEAM (TE = 10, 20, 30, 40, and 50 ms)	IDEAL		r2 = 0.99
Georgoff et al[69]	2012	Prospective	50.6	52	Steatosis	3.0 T. PRESS (TE = 50 ms)	Liver biopsy	15 ± 9 d	Diagnostic accuracy was (AUC: 0.95; 95%CI: 0.89–1.0)
Kang et al[18]	2012	Prospective	54	56	Steatosis	1.5 T. STEAM (TE = 20, 30, 40, 50, and 60 ms)	Liver biopsy	1–28 d	r = 0.95
Parente et al[70]	2014	Prospective	54 ± 9	73	Nonalcoholic fatty liver disease	3.0 T. PRESS (TE = 40 ms)	Liver biopsy		r = 0.767; P < 0.001
Bashir et al[71]	2015	Prospective	55 ± 13.8	217	Various hepatic diseases	1.5 T. STEAM (TE = 12 ms)	Two-point Dixon		r = 0.61; P < 0.001
Kim et al[57]	2015		52.8 ± 14	42	Various hepatic diseases	3.0 T. STEAM (TE = 12, 24, 36, 48, and 72 ms)	In- and opposed-phase echo pairs		r = 0.97
Satkunasingham et al[72]	2015	Retrospective	57.8 (12–83)	156	Various hepatic diseases	3.0 T. STEAM (TE = 12, 24, 36, 48, and 72 ms)	MRI-PDFF		r = 0.977; P < 0.001
Rastogi et al[73]	2016	Retrospective	32.5	73	Steatosis	3.0 T. STEAM (TE = 15, 20, 25, 30, and 35 ms)	Biopsy and surgery	≤ 20 d	MRS correlated well with the histopathology results (r = 0.882). An accuracy of 96% and sensitivity of 94%
Kramer et al[6]	2017	Prospective	57 ± 5	50	Various hepatic diseases	1.5 T. STEAM (TE = 10, 20, 30, 40, and 50 ms)	PDFF		r2 = 0.992; slope, 0.974; intercept, –0.943

MRS: Magnetic resonance spectroscopy; PDFF: Proton density fat fraction; TE: Echo time; BMI: Body mass index; CT: Computed tomography; Blank: No information; PRESS: Point-resolved spectroscopy; STEAM: Stimulated-echo acquisition mode.

Table 2 Studies reporting on the measurement of the hepatic fat content with in-phase and out-of-phase imaging versus liver biopsy and other imaging methods

Ref.	Year	Study design	Age (year)	N	Etiology	Field strength sequence	Comparison	Interval	Results
Fishbein et al[35]	2005		47 ± 10	38	Various hepatic diseases	1.5 T. IP/OP (Dixon)	Biopsy	2 wk	r = 0.773, P < 0.001; Macrovesicular steatosis: r = 0.920, mixed steatosis: r = 0.605, P = 0.05
Kalra et al[74]	2009	Prospective	41 ± 9.2	10	Nonalcoholic fatty liver disease	1.5 T. IP/OP (Dixon)	Biopsy		Provides data on fat infiltration without information of hepatic fibrosis
Mennesson et al[41]	2009	Prospective	52.5	40	Various hepatic diseases	1.5 T. IP/OP (Dixon)	Biopsy	Same day	r = 0.852; P < 0.0001
Fischer et al[37]	2010	Prospective	66 ± 12	23	Various hepatic diseases	1.5 T IP/OP (Dixon)	Biopsy and surgery	≤ 10 d	r = 0.92; P < 0.0001
Pacifico et al[75]	2011	Case–control	7-16	25	Nonalcoholicfatty liver disease	1.5 T. Two-point Dixon	Biopsy	1–7 d	r = 0.883; P < 0.0001
Guaraldi et al[76]	2012	Observational pilot		16		1.5 T. IP/OP (Dixon)	Biopsy		r = 0.88; P < 0.0001
Koelblinger et al[77]	2012	Prospective	60.5	35	Various hepatic diseases	3.0 T. IP/OP (Dixon)	Biopsy		Uncorrected: r = 0.67, P < 0.001. Spleen correction: r = 0.85, P < 0.001
Rastogi et al[73]	2016	Retrospective	32.5	73	Steatosis	3.0 T. IP/OP (Dixon)	Biopsy and surgery	≤ 20 d	Dual-echo MRI correlated well with the histopathology results (r = 0.871). An accuracy of 95% and sensitivity of 97%
Bhat et al[78]	2017	Prospective	46	30	Steatosis	1.5 T. Two-point DIXON	Biopsy	1 wk	Good correlation between the MR estimation of liver fat and histological grading. 90% of patients had a fat content of less than 10%. The maximal fat content of 28% was observed in one patient

MRI: Magnetic resonance imaging; Blank: No information.

Table 3 Studies reporting on the measurement of the hepatic fat content with multiple-point Dixon imaging versus liver biopsy and other imaging methods

Ref.	Year	Study design	Age (year)	N	Etiology	Field strength sequence	Comparison	Interval	Results
Noureddin et al[79]	2013	Randomized		50	Nonalcoholic fatty liver disease	MRI-PDFF	MRS	0 and 24 wk	r2 = 0.98; P < 0.0001
Idilman et al[28]	2013	Prospective	44.7 ± 13.1	70	Nonalcoholic fatty liver disease	1.5 T. IDEAL-IQ	Biopsy	14.5 d (0–259)	r = 0.820; The correlation of PDFF in mild hepatic steatosis was found to be better than that of moderate or severe steatosis (r = 0.835 and r = 0.402, respectively; P = 0.003)
Deng et al[51]	2014	Prospective	3–16	10	Nonalcoholic fatty liver disease	1.5 T. Multi-point Dixon	Biopsy		r = 0.90; P = 0.0004
Kukuk et al[59]	2015		51.7 ± 15.2	59	Liver disorders	3.0 T. Six echo-mDixon	Biopsy	≤ 6 wk	r = 0.967, P < 0.001. Slightly a higher hepatic fat contents than q Histo (mean difference 2.1% for 6E-mDixon and 1.9% for MRS)
Rehm et al[52]	2015	Prospective	13.3 ± 2 (11–22)	132	Healthy females	3.0 T. Multi-echo Dixon	STEAM (TE = 10, 15, 20, 25, and 30 ms)		r = 0.96
Schwimmer et al[80]	2015	Prospective	14	174	No steatosis and nonalcoholic fatty liver disease	3.0 T. Multi-echo Dixon	Biopsy	57 ± 51 d	r = 0.725; P < 0.01
Idilman et al[55]	2016	Retrospective	41.7 ± 14.6	19	Nonalcoholic fatty liver disease	1.5 T. DEAL-IQ	Biopsy		r = 0.743; P < 0.001
Hetterich et al[39]	2016	Prospective	57.2 ± 9.4	215		3.0 T. STEAM (TE = 12, 24, 36, 48, and 72 ms)	Multi-echo Dixon		r = 0.96; P = 0.001
Middleton et al[81]	2017	Randomized	51 ± 11	113	Nonalcoholic steatohepatitis	1.5 T or 3.0 T. Six echo-mDixon	Biopsy	51 d	r = 0.80; P < 0.001
Kang et al[46]	2018	Prospective	47.3 ± 14.9	29	NAFLD (34). Alcoholic liver disease (13). Liver cirrhosis (9)	3.0 T. mDIXON-Quant sequence	Biopsy	Same day	r = 0.809; P < 0.001
Pickhardt et al[82]	2018	Retrospective	54 ± 12	221		1.5 T or 3.0 T. MRI-PDFF	CT	0–158 mo	r = 0.88 (≤ 1 mo) substantially worsened with increasing time
Guo et al[83]	2020	PProspective	52.6 (22–83)	400	Healthy adults and older adults	3.0 T mDixon-Quant sequence	CT	Same day	r = 0.79; P < 0.001

MRS: Magnetic resonance spectroscopy; PDFF: Proton density fat fraction; TE: Echo time; BMI: Body mass index; CT: Computed tomography; Blank: No information; PRESS: Point-resolved spectroscopy; STEAM: Stimulated-echo acquisition mode.