ORIGINAL ARTICLE

Liver Steatosis Quantification Using Magnetic Resonance

Imaging: A Prospective Comparative Study With Liver Biopsy
Nicolas Mennesson, MD,* Jerome Dumortier, MD, PhD, Valerie Hervieu, MD, Laurent Milot, MD,*
Olivier Guillaud, MD, Jean-Yves Scoazec, MD, PhD, and Frank Pilleul, PhD, MD*
Background and Aims: To prospectively determine the accuracy
of liver fat quantication with magnetic resonance imaging (MRI).
Patients and Methods: The population consisted of 40 patients
(mean age, 52.5 years; range, 23Y78 years). The same day, all patients
underwent MRI and ultrasonography-guided liver biopsy. The histological evaluation of steatosis was performed by an experienced liver
pathologist blinded to the MRI results. On T1-weighted in- and opposedphase images, one radiologist, experienced in abdominal imaging,
blinded to the clinical and pathological results, recorded signal intensity
(SI) by mean regions of interest placed at same locations in both phases.
Fat-water ratio was obtained by dividing SI of liver in opposed-phase
sequence by SI of liver in in-phase sequence. The fat-water ratio and
the histological grade of steatosis were compared by linear regression.
Receiver operating characteristic curve was used to dene the sensitivity and specicity of fat-water ratio as a diagnostic tool for evaluation of
steatosis.
Results: Diagnoses were nonalcoholic fatty liver disease (n = 25),
alcoholic liver disease (n = 10), cholangiopathy (n = 2), and autoimmune
hepatitis (n = 3). Fatty liver inltration was present in 80% of patients.
The mean (SD) percentage of fatty hepatocytes was 38.7% (29.2).
Fat-water ratio and steatosis grade were highly correlated (r = 0.852,
P G 0.0001). Sensitivity and specicity of fat-water ratio to detect fatty
inltration greater than 20% were 96% and 93%, respectively.
Conclusions: This prospective study demonstrates that MRI can be
proposed as a noninvasive method to screen and quantify liver steatosis.
Key Words: MRI, liver, steatosis, detection
(J Comput Assist Tomogr 2009;33: 672Y677)

atty inltration of the liver or steatosis is a common indicator

of hepatocellular lesion secondary to a variety of etiologies.
One of the most common causes of steatosis in developed
countries is nonalcoholic fatty liver disease (NAFLD), mainly
characterized by the occurrence of macrovesicular steatosis in
the absence of signicant alcohol consumption. Nonalcoholic
fatty liver disease encompasses a broad range of histological
lesions, from isolated steatosis to nonalcoholic steatohepatitis
(NASH), in which steatosis is associated with various degrees of
inammation, brosis, and ballooning degeneration of hepatocytes. The pathogenesis of NAFLD is multifactorial, in the
context of the so-called metabolic syndrome,1 combining obesity, diabetes, hypertension, and hypertriglyceridemia, 2
and associated with insulin resistance. So far, liver biopsy is re-

From the *Service de Radiologie Digestive, Federation des Specialites

Digestives, and Service Central dAnatomie et Cytologie Pathologiques,
Hopital Edouard Herriot, Hospices Civils de Lyon, Lyon, France; and
Universite Claude Bernard Lyon 1, Villeurbanne, France.
Received for publication September 25, 2008; accepted December 22, 2008.
Reprints: Frank Pilleul, PhD, MD, Service de Radiologie Digestive, Pavillon
H, Hopital Edouard Herriot, Place dArsonval, 69003 Lyon, France
(e-mail: frank.pilleul@chu-lyon.fr).
Copyright * 2009 by Lippincott Williams & Wilkins

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quired when an assessment of activity and severity of NAFLD

is considered necessary.
In the United States, approximately 47 million individuals
are estimated to have a metabolic syndrome3: fatty inltration
of the liver can be detected in up to 12% to 15% in this population,4 and 3% to 4% of patients with NAFLD have steatohepatitis. Nonalcoholic steatohepatitis was originally believed to
be a benign disease. However, it has been recently shown that
NASH could lead to irreversible liver disease in some patients.5
In addition, when another liver disease is present, coexistent
steatosis may exacerbate liver injury by acting as a cofactor.
Therefore, the diagnosis of steatosis does have important therapeutic implications, because active management of obesity and
a reduction in steatosis may improve liver injury and decrease
the progression of brosis. This prompts a considerable interest
in the development of noninvasive methods for the detection and
quantication of the fatty inltration of the liver in the context
of NAFLD. Moreover, after a rst biopsy to diagnose NAFLD
or NASH, a noninvasive, safe, reproducible technique of quantication could allow for the evaluation of the effects of NAFLD
treatment without the need of a liver biopsy. In such indications,
not only qualitative but also quantitative information would be
important.
It has been shown that several noninvasive techniques
such as ultrasonography (US), computed tomography (CT), and
magnetic resonance imaging (MRI) can detect liver steatosis.
Ultrasonography is widely used to detect hepatic steatosis, but
its sensitivity is reduced in patients with small amounts of fatty inltration; moreover, it cannot provide reliable quantitative
data. Unenhanced CT can detect and characterize macroscopic
fat in the liver using liver-to-spleen attenuation difference with
excellent correlation in patients with more than 30% of steatosis;
however, the feasibility and reliability of a quantitative evaluation with this method remain to be demonstrated.
The purpose of the present study was therefore to determine
the accuracy of MRI in the detection and quantitative assessment
of the extent of liver steatosis, as compared with histological
evaluation.

MATERIALS AND METHODS

Patient Selection and Study Design
This was a prospective single-institution study. The study
protocol was approved by the human research committee of our
institution. After the risks and possible benets of the procedure
were fully explained, all patients gave written informed consent
and signed an institutional review boardYapproved, Health Insurance Portability and Accountability ActYcompliant consent
form before MRI. Forty asymptomatic patients (20 women and
20 men; mean age, 52.5 years; range, 23Y78 years), with an
incidentally discovered elevation of liver enzymes, no history
of excessive alcohol intake, negative results of viral screening,
and no liver mass at US, were referred for liver biopsy for diagnostic purposes between April 2007 and February 2008 and
were included in the study.

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Clinical Data Collection

Physical Examination
Body measurements included weight and standing height
at the time of liver biopsy. Body mass index (BMI, kilograms
per square meter) was calculated from these values. Obesity was
dened as a BMI 30 kg/m2 or more and overweight as a BMI
25 kg/m2 or more for a man or 24 kg/m2 or more for a woman.

Associated Diseases
The occurrence of diabetes, arterial hypertension, hyperlipidemia, and/or regular alcohol consumption was checked for.

Laboratory Assessments
Biological data including hematological parameters, liver
function tests, coagulation tests, renal parameters, and fast blood
glucose and lipid proles were obtained the same day than liver
biopsy.

Magnetic Resonance Imaging

Magnetic Resonance Imaging Technique
Magnetic resonance imaging and liver biopsy were performed the same day, and to avoid postYbiopsy artifacts, MRI
was the rst procedure to be performed. Magnetic resonance
imaging was performed with a 1.5-T superconducting magnet
(Magnetom Symphony; Siemens Medical Systems, Erlangen,
Germany) and a 4-element phased-array body coil (Siemens
Medical Systems). Nonenhanced transverse T1-weighted in-phase
(IP) and opposed-phase (OP) breath-hold spoiled gradient-echo
(GRE) MRI sequences were performed with repetition time of
181 milliseconds/echo time of 2.38 milliseconds (OP imaging)
and 4.76 milliseconds (IP imaging), ip angle of 70 degrees,
section thickness of 6 mm, intersection gap of 0 mm, matrix of
256  110, eld of view of 400 cm2, phase eld of view of 62.5%,
and time acquisition of 23 seconds.

Liver Steatosis Quantification Using MRI

recorded as the mean of the 3 regions of interest. Fat-water ratio

was quantied on T1-weighted GRE MRIs as the percentage of
relative SI loss of the liver on OP images, with the following
formula: (SI in Y SI out) / (SI in + SI out), as SI out denotes out-ofphase SI, and SI in denotes IP SI, where SI in = W + F and SI out =
W j F (W and F denote water and fat vectors, respectively).

Histopathology
Percutaneous liver biopsies were performed with a 14gauge needle, under US guidance, along the midaxillary line,
in variable segments in the right hepatic lobe. All biopsies were
1.5 cm or more in length. Tissue samples were xed in buffered
formalin and embedded in parafn. Sections, 4 Km thick, were
stained with hematoxylin-eosin-saffron, Perls iron stain, and
chromotrope and evaluated by one pathologist. The histopathological evaluation was performed masked from any clinical information. Furthermore, liver steatosis was reported as a
quantitative evaluation of the percentage of hepatocytes (0%Y
100%), containing macrovesicular fat (fat droplets equal to or
larger than the size of the nucleus, often displacing the nucleus)
or microvesicular fat (numerous small fat droplets surrounding
a centrally located nucleus). The following grading system was
used for reporting: grade 0, less than 5% of steatotic hepatocytes; grade 1, 6% to 33%; grade 2, 34% to 66%; and grade
3, greater than 66%. In addition, the distribution of steatosis
within the lobule (zone 3 predominant, zone 1 predominant,
panlobular, and azonal) was noted. Fibrosis was evaluated on
chromotrope-stained slides according to the Brunt classication6: 0 (none), 1 (perinusoidal or portal/periportal), 2 (perisinusoidal and portal/periportal), 3 (bridging brosis), and 4
(cirrhosis). A diagnostic of NASH was considered when the
NAFLD activity score (NAS; Table 1), as previously dened,7
was more than 5.

Statistical Analysis
To determine whether MRI could be able to give a quantitative evaluation of the extent of hepatic steatosis, hepatic fat

Image Interpretation
One radiologist (N.M.) who was unaware of clinical examination, history, and pathological results interpreted MR examinations on a picture archive and communication system
workstation (Impax; Agfa, Mortsel, Belgium) by using qualitative and quantitative methods to determine the presence and
degree of hepatic steatosis.
Qualitative Assessment
Overall image quality was evaluated subjectively. The presence of fatty inltration was determined based on characteristic
signal features, recognized as regions of the liver that demonstrated a decrease in signal intensity (SI) on OP images as compared with IP images. The spleen and skeletal muscle were used
as reference tissues for SI changes because they are known to
contain little intracellular lipid.
Region-of-Interest Analysis
Signal intensity from regions of interest in the liver was
recorded for T1-weighted IP and OP GRE sequences. Three
different regions of interest were drawn in liver segments 5, 7,
and 8 for each patient. These regions of interest were drawn
so as to be more than 1.5 cm2 to include representative areas of
parenchyma that did not contain blood vessels or an artifact and
to be potentially at a similar location and depth of the liver biopsies. For each sequence, the region of interest in the liver parenchyma was matched on the same location, taking care to avoid
areas with vessels and motion artifacts. The SI of the liver was
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TABLE 1. Histological Scoring System for NAFLD

Steatosis

Lobular inflammation

Hepatocyte ballooning

Fibrosis

Score

Extent

0
1
2
3
0
1
2
3
0
1
2
0
1
1A
1B
1C
2
3
4

G5%
5Y33%
933Y66%
966%
No foci
G2 foci/200
2Y4 foci/200
94 foci/200
None
Few balloon cells
Many cells/prominent ballooning
None
Perisinusoidal or periportal
Mild, zone 3, perisinusoidal
Moderate, zone 3, perisinusoidal
Portal/periportal
Perisinusoidal and portal/periportal
Bridging fibrosis
Cirrhosis

Components of NAS and brosis staging.

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TABLE 2. Results of Histological Examination

All Patients
Steatosis
Fibrosis stage

Patients With NAFLD

Other Pathology

Mean (SD)

Mean (SD)

Mean (SD)

33
37

39% (29)
1.94 (1.17)

18
18

45% (28)
2.17 (1.1)

15
18

29% (25)
1.8 (1.19)

fraction and fat-water ratio were correlated with the histological

degree of steatosis by using a linear regression analysis and Pearson correlation coefcient (r) (XL stat-Pro for Excel; Addinsoft,
Paris, France). The degree of steatosis, as determined by the pathologist, was used as a continuous variable in the regression
models because the value of the hepatic fat fraction and the fatwater ratio that were calculated by using the MRIs was a continuous variable.
The overall diagnostic performance of diagnosis of liver
steatosis was compared with that of fat-water ratio by receiver
operating characteristic analysis. A receiver operating characteristic curve was produced to demonstrate the sensitivity and
specicity of this parameter in our population and has been used
to assess the accuracy of the dual fast GRE as a diagnostic test
in liver steatosis using a threshold value of 5% for the pathological analysis and 20% in case of surgical approach.

RESULTS
Clinical and Biological Results
The nal diagnoses of the conditions of the patients in the
study group (as assessed from the combination of clinical, biological, and histological data) were NAFLD in 18 patients (including 10 patients with NASH), alcoholic steatohepatitis in 9,
cholangiopathy in 3, autoimmune hepatitis in 4, drug-induced
steatohepatitis in 1, hemochromatosis in 1, and cryptogenetic
liver disease in 4.
An elevated BMI was present in 29 (72.5%) of 40 patients.
From these patients, 17 (58.6%) had a diagnosis of NAFLD.
The mean (SD) BMI values were 32 (7.5) kg/m2 in patients with
NAFLD and 26 (4.4) kg/m2 in others.
Mean aspartate aminotransferase level was 60.2 UI/L (n =
10Y45), and mean alanine aminotransferase level was 66.4 UI/L
(n = 10Y45). Mean bilirubin level was 32.9 Kmol/L (n G 20).
Mean triglyceride level was 4.8 mmol/L (n G 2), and mean cholesterol level was 5.8 mmol/L (n = 3.5Y6.5). Diabetes was diagnosed in 12 (60%) of the patients with NAFLD and 25% of
the others.

series. Dropout SI on T1-weighted OP GRE sequence was identied in 37 patients.

The mean (SD) fat-water ratio of SI between T1-weighted
OP and IP images was 0.196 (0.075; P G 0.0001). The mean
(SD) fat-water ratios were 0.31 (0.22) in the subgroup of patients
with histological evidence of fatty liver inltration and 0.00
(0.06) in the subgroup of patients without liver fatty inltration
at histological examination (P G 0.0001). We then compared
the median fat-water ratio according to the histological grade
of steatosis: j0.014 (j0.013 to 0.027) for grade 0; 0.026 (0.001
to 0.150) for grade 1; 0.243 (0.065 to 0.313) for grade 2; and
0.506 (0.185 to 0.694) for grade 3. The differences were statistically signicant between grades 0 and 1 (P G 0.01), grades 1
and 2 (P G 0.01), and grades 2 and 3 (P G 0.01).
At individual level, the fat-water ratio was strongly correlated with the histological evaluation of steatosis (P G 0.0001),
the coefcient of linear regression corresponding to r = 0.852
(Fig. 1). The relation between the histological degree of steatosis
and the fat-water ratio can therefore be expressed by the following formula: %Steatosis = ((106.6)  (fat-water ratio)) + 17.8.
Fat-water ratio (cutoff value 9 0) had a sensitivity of 97%
and a specicity of 86% for the diagnosis of steatosis greater
than 5% (Fig. 2A). Fat-water ratio (cutoff value 9 0.037) had a
sensitivity of 96% and a specicity of 93% for the diagnosis of
steatosis greater than 20% (Fig. 2B).

DISCUSSION
Nowadays, liver biopsy remains the criterion standard
for accurately determining, in a semiquantitative manner, the
amount of fatty liver inltration. Furthermore, liver biopsy is
able to detect subclinical hepatic pathologies associated with
steatosis and contribute to the etiological and differential diagnoses. Liver biopsy is able to evaluate lesions associated with
steatosis, such as brosis and inammation, and therefore to

Histological Results
Liver steatosis was present in 33 patients (82.5%).
Histological gradings were 0 in 7 patients, 1 in 10 patients, 2
in 12 patients, and 3 in 10 patients (Table 2). The mean (SD)
percentage of steatosis was 38.7% (29.2; range, 0%Y90%).
Macrovesicular steatosis was present in 26 patients (79%) and
microvesicular steatosis in 2 patients (6%); an association of
macrovesicular and microvesicular steatoses was observed in 5
patients (15%). Thirty-six patients presented with liver brosis:
score 1 in 17 patients (42.5%), score 2 in 9 patients (22.5%),
score 3 in 4 patients (10%), and score 4 in 6 patients (15%). Ten
patients with NAFLD (50%) had a NAS of 5 or greater and were
therefore considered to have NASH (Table 1).

Magnetic Resonance Imaging Results

T1-weighted IP and OP GRE sequences were obtained in
all 40 patients; there were no cases of technical failure in this

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FIGURE 1. Relation between histological fatty liver inltration and

fat-water ratio.
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Liver Steatosis Quantification Using MRI

MRI sequences facilitate in the detection of fat, including fat

suppression sequences and chemical shift imaging with OP
GRE sequences.4 At 1.5 T, lipid and water protons precess IP
approximately every 4.2 milliseconds (IP imaging), and our
signals are additive. Imaging during intermediate echo times of
approximately 2.1 milliseconds (OP imaging) leads to phase
cancellation effect at a voxel level, resulting in loss of signal in
voxel with fat and water. Thus, appropriate selection of echo
time can be used to obtain images with differing relative contributions of fat and water signals. In-phase and OP GRE sequences are useful techniques for the diagnosis of diffuse or
focal hepatic steatosis.9Y12 Therefore, we evaluated this simple
powerful technique to quantify liver steatosis. The IP and OP
images were measured simultaneously with a clinical dual GRE
sequence including a breath-holding technique in the same region of the liver. The entire liver with the GRE sequence was
scanned in 22 seconds during a breath-hold.
Our results highlight the performances of this MR sequence
for the diagnosis and evaluation of liver steatosis (Fig. 3A,B).
For fatty inltration of more than 20%, sensitivity and specicity
of MR fat quantication were 96% and 93%, respectively. This

FIGURE 2. A, Receiver operating characteristic curves show ability

of fat-water ratio to reveal 20% of liver steatosis. B, Receiver
operating characteristic curves show ability of fat-water ratio to
reveal 5% of liver steatosis.

evaluate the stage and grade of the disease. However, percutaneous liver biopsy is an invasive procedure and is not devoid
from mortality and morbidity.8 Furthermore, heterogeneity in
the distribution and amount of steatosis may be responsible for
signicant biases of evaluation owing to sampling error.
A reliable noninvasive method for the evaluation of fatty
liver inltration would be a very signicant improvement for the
screening of patients at risk for liver steatosis such as NAFLD,
the long-term monitoring of patients with the disease, and the
evaluation of the results of dedicated therapeutic interventions.
Our prospective study strongly suggests that MRI should be an
interesting tool fullling these requirements.
At imaging, the diagnosis of liver steatosis is currently
based on qualitative rather than quantitative procedures. Fatty
liver inltration usually appears hyperechoic at US and is of low
attenuation compared with normal liver parenchyma at
CT, with a range of j10 to j100 HU. On MRI, fat liver appears high in SI on T1-weighted images.3 In addition, several
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FIGURE 3. Transverse IP (A) and OP images (B) of the liver in a

patient suspected of having NASH. Signicant dropout SI of the
liver between the IP (A) and OP (B) images. The fat-water ratio was
0.09, and the MR quantication of fatty liver inltration was 83%
using the equation in comparison to 80% by the histological
evaluation. A 49-year-old woman with liver steatosis presented a
BMI of 37 kg/m2, aspartate aminotransferase level of 81 UI/L,
alanine aminotransferase level of 136 UI/L, and NASH syndrome at
nal diagnosis.
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Mennesson et al

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was observed irrespectively of the etiology of the underlying

chronic liver diseases: chronic viral hepatitis, alcoholic fatty liver disease, and NAFLD. Our results compare favorably to those
reported with other imaging techniques.
According to Saadeh et al,13 steatosis could be reliably
detected, with high sensitivity of 100% and 93% but low positive
predictive values of 62% and 76% for US and CT, respectively.
Recently, Fishbein et al14 reported that MRI is superior to US
in detecting and quantifying minor degrees of fatty metamorphosis in the liver. Ricci et al,15 using CT that was performed
without contrast material enhancement, reported a correlation
coefcient of 0.83 between the percentage of the liver fat and
the ratio of the density of the liver to that of the spleen. Limitations of US and CT include the inability to aid in distinguishing between brosis and fat with US and the masking effect
of factors that increase liver density, such as the presence of
iron, copper, glycogen, or amiodarone-induced phospholipidosis, with CT.16 In addition, CT is difcult to use for quantitative
evaluation of fat liver inltration; this requires specic protocols
and depends on the type of CT used, the contrast volume, the
injection rate, and the type of contrast used17,18. Finally, classic
CT methods, either in terms of[in, of ,for] absolute Hounseld
units of the liver or as liver-to-spleen ratio, may suffer from
uctuations related to the volume, the noise of the patients and
the shape of both the liver and spleen.
A simple and reliable tool for fatty liver quantitation remains therefore needed. Our prospective study provides convincing data to validate a noninvasive test that could be used
widely in MR clinical study for the assessment of liver steatosis.
A signicant correlation was found between the degree of steatosis on histological examination and the fat-water ratio on
MRI. Furthermore, we demonstrated signicant differences in
the value of fat-water ratio according to the grade of steatosis
at histological examination. Even if the small number of patients
included in our study and the heterogeneity of underlying pathologies must be taken into account, the results obtained are
highly encouraging and provide a rm basis for stimulating further studies including a larger number of patients. Moreover, our
results in a nonselected population of patients are concurrent
with those of Rinella et al10,11 and more recently Kim et al12 in
one specic indication: predicting the appropriateness of liver donation in candidate living liver donors. These studies concluded
that liver biopsy can be obviated in such cases and that donor
selection might be more accurate than biopsy because the latter
is limited by sampling error (Fig. 3A,B). A particularly interesting clinical application of MRI would be the monitoring of
liver steatosis in patients under targeted medical treatment, parenteral nutrition or after bariatric surgery, without performing
iterative liver biopsies.19,20
Chemical shift MRI has some technical limitations. This
especially includes the ambiguity error.21 Because the OP images accurately reect the differences in water and fat signals, it
is supposedly not possible to determine whether fat or water is
the dominant signal. Although this error should inuence measurements in areas with very abundant steatosis, this paradoxical
increase in the signal did not occur in our study.
Another point to underline is that fat content is not the only
determinant of liver disease. Other factors, which have not been
evaluated in this study, such as brosis and hepatocellular necrosis, are essential in the progression of chronic liver disease. It
is too early to evaluate whether such parameters could be determined in the future by using noninvasive imaging techniques.
However, it must be acknowledged that biological markers and
scores have been proposed to characterize NAFLD and NASH,
with a specic focus on brosis and inammation, rather than

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steatosis.22,23 Recently, Poynard et al24 evaluated a panel of biomarkers (SteatoTest) for the noninvasive diagnosis of steatosis
in patients with or without chronic liver disease. SteatoTest
was constructed using a combination of the 6 components of
FibroTest-ActiTest, BMI, and serum cholesterol, triglyceride,
and glucose levels adjusted for age and sex. The median SteatoTest value was 0.31 in patients without steatosis, 0.39 in grade 1
steatosis (0%Y5%), 0.58 in grade 2 (6%Y32%), and 0.74 in
grades 3 and 4 (33%Y100%). It would be interesting to compare
the results and the cost/benet ratio of biochemical techniques
with MRI and to evaluate the interest of combining the various
noninvasive techniques currently under evaluation in some specic indications.
In conclusion, our study strongly suggests that the comparison of T1-weighted IP and OP GRE images is an efcient
method for the diagnosis and quantication of liver steatosis
with only 1 short TR series.
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