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Noninvasive detection of hepatic steatosis in

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1330 Original article

Noninvasive detection of hepatic steatosis in patients without

ultrasonographic evidence of fatty liver using the controlled
attenuation parameter evaluated with transient elastography
Yusuf Yilmaza,c, Rabia Ergelenb, Hakan Akina,c and Nese Imeryuza,c
Objective Although ultrasound is a useful technique
for detecting hepatic steatosis, it cannot provide a precise
determination of hepatic fat content. A novel attenuation
parameter named controlled attenuation parameter
(CAP) has been developed to process the raw ultrasonic
signals acquired by Fibroscan. The aim of this study
was to determine the percentage of hepatic steatosis
in apparently healthy Turkish individuals using the
proposed diagnostic cut-off points for CAP. In addition,
we sought to investigate the association of CAP with the
traditional risk factors for nonalcoholic fatty liver disease in
a screening setting.
Materials and methods In the present study, 102 Turkish
individuals without evidence of fatty liver on ultrasound
and normal aminotransferase levels underwent CAP
measurements by means of Fibroscan.
Results The mean (SD), median (minimum maximum),
and 5th and 95th percentile values of CAP values in
this cohort of 102 individuals were 206.99 (48.12), 210.5
(100.0 314.0), 113.4 and 280.2 dB/m, respectively. Using
the cut-offs of 222, 238, and 283 dB/m for CAP, there

Introduction
Nonalcoholic fatty liver disease (NAFLD) traditionally
defined as the accumulation of triglycerides within the
cytoplasm of hepatocytes that exceeds 5% of liver weight
in the absence of significant alcohol use is the most
common form of metabolic liver disorder in the general
population worldwide [13]. Current estimates in the
USA indicate that NAFLD can be identified on imaging
in 2033% of adults and in 316% of potential liver
donors [1,4]. NAFLD is generally considered the result of
states of insulin resistance (such as the metabolic
syndrome and obesity) on the hepatic metabolism [5,6].
Consistent with the obesity epidemic, the data from the
United Network for Organ Sharing have suggested that
the proportion of liver transplants involving patients with
nonalcoholic steatohepatitis (NASH) increased from
1.2% from 1997 to 2003 to 7.4% in 2010, making NASH
the fourth most common reason for liver transplantation [7]. Remarkably, there is emerging consensus that
NAFLD will become the leading indication for liver
transplantation within the next 1020 years, surpassing
the current leader, hepatitis C virus infection [8,9].
The lack of consistency in diagnostic tests to identify
NAFLD and its different clinical expressions (i.e. simple
c 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins
0954-691X

were 39 (38.2%), 23 (22.5%), and five (4.9%) individuals

out of 102 who had at least 10% steatosis despite normal
liver findings on ultrasound. After allowance for potential
confounders, CAP was independently associated with BMI
(b = 0.39, t = 3.5, P < 0.001) and the number of metabolic
syndrome criteria (b = 0.24, t = 2.1, P < 0.05).
Conclusion These results hold promise for early
noninvasive detection of hepatic steatosis on the
basis of CAP assessment. Eur J Gastroenterol Hepatol
c 2013 Wolters Kluwer Health | Lippincott
25:13301334
Williams & Wilkins.
European Journal of Gastroenterology & Hepatology 2013, 25:13301334
Keywords: controlled attenuation parameter, Fibroscan, hepatic steatosis,
nonalcoholic fatty liver disease
Departments of aGastroenterology, bRadiology, School of Medicine and cInstitute
of Gastroenterology, Marmara University, Istanbul, Turkey
Correspondence to Yusuf Yilmaz, MD, Institute of Gastroenterology, Marmara
University, P.K. 53, Basibuyuk, Maltepe, 34840 Istanbul, Turkey
Tel: + 90 533 4403995; fax: + 90 216 6886681;
e-mail: dryusufyilmaz@gmail.com
Received 28 February 2013 Accepted 15 April 2013

steatosis and NASH) has been a major scientific and

clinical issue [1012]. Although liver biopsy is considered
to be the gold standard for the diagnosis of NAFLD, its
invasiveness has led to cases of morbidity and mortality [13,14]. As a consequence, several imaging techniques
(including ultrasound, MRI, computed tomography, and
proton magnetic resonance spectroscopy) have been
proposed as a replacement for, or to be used in
combination with, histopathological analysis of liver
biopsies [15,16]. Ultrasound is the most commonly used
imaging modality for subjects with suspected NAFLD
[17]. The typical criteria for fatty liver on ultrasound are
liver brightness, deep attenuation, vascular blurring, and
hepatorenal echo contrast. Although ultrasound is a
useful technique for detecting hepatic steatosis, particularly in severe cases (steatosis > 30%), it is operatordependent and cannot provide a precise determination of
hepatic fat content, especially if steatosis is less than
30% [16,17].
A novel attenuation parameter called controlled attenuation parameter (CAP) has been developed to process the
raw ultrasonic signals acquired by the Fibroscan (Echosens SA, Paris, France), which is an ultrasound-based
device used to diagnose liver disease [1823]. Growing
DOI: 10.1097/MEG.0b013e3283623a16

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Steatosis on transient elastagraphy Yilmaz et al. 1331

evidence suggests that fat impedance is greater than the

one of soft tissues and hence in the presence of steatosis,
the ultrasound signal will be attenuated [22,23]. Therefore, CAP values are not only higher among patients with
significant fatty liver infiltration but this index can also
very efficiently detect even low-grade steatosis [1823].
Sasso et al. [18] reported that CAP showed an area under
receiver-operative characteristic curve of 0.91 and 0.95 for
the detection of more than 10 and 33% of steatosis,
respectively. In this cohort, a CAP cut-off of 238 dB/m
was 91% sensitive and 81% specific for the detection of
steatosis [18]. The CAP has also been shown to have a
good ability to differentiate steatosis grades in patients
with chronic hepatitis C [20]. In these patients, a
threshold of 222 dB/m was 76% sensitive and 71% specific
for detecting hepatic steatosis [20]. Myers et al. [21]
reported that at a cut-off of 283 dB/m, the CAP was 76%
sensitive, 79% specific, and had positive and negative
predictive values of 87% and 64%, respectively, for the
diagnosis of steatosis.
To the best of our knowledge, the usefulness of CAP as a
screening tool for detecting hepatic steatosis in apparently healthy individuals has not yet been evaluated. To
obtain an acceptable normal range for CAP, this index
needs to be explored in ethnically diverse healthy populations. In the present study, we measured CAP values
in a sample of healthy Turks and compared the values
with the proposed diagnostic cut-off points for the
presence of hepatic steatosis. In addition, we sought to
investigate the association of CAP with the traditional
risk factors for NAFLD in a screening setting.

Materials and methods

209.1 and 358.15 dB/m, respectively. In a second step,

two individuals were excluded because of increased ALT,
one because of HBsAg (+), 12 because of a diagnosis of
the metabolic syndrome, and two because of alcohol
drinking. Finally, we excluded two patients with LSM
failures and four unreliable examinations. LSM failure
was defined as zero valid shots and unreliable examinations were defined as fewer than 10 valid shots, an
interquartile range/LSM greater than 30%, or a success
rate less than 60% [25]. Therefore, a total of 102
individuals (64 women and 38 men, mean age 359
years) were included in the final analysis (Fig. 1). Blood
pressure was measured using a mercury sphygmomanometer in a quiet room after at least a 10-min rest. Korotkoff
1 and 5 were taken for systolic blood pressure and

Fig. 1

Initial cohort
screened by
ultrasound (n = 165)

Excluded because of
steatosis on ultrasound
(n = 40)

Screening for
elevated
ALT, HBsAg (+),
metabolic
syndrome,
alcohol drinking
(n = 125)

Excluded because of
ALT > 42 U/l (n = 2);
HBsAg (+) (n = 1);
metabolic syndrome (n = 12);
alcohol drinking (n = 2)

Individuals who
underwent
Fibroscan
examination
(n = 108)

Excluded because of
liver stiffness
measurement
failures (n = 2) or
unreliable examinations
(n = 4)

Study participants

In the present study, liver stiffness measurement (LSM)

and CAP were assessed by Fibroscan in 165 Turkish
individuals recruited from among hospital staff or patients
without chronic liver disease (e.g. patients with dyspepsia). The exclusion criteria were as follows: presence of
hepatic steatosis on ultrasound, a diagnosis of the
metabolic syndrome according to the ATP III criteria [24], age less than 18 years or more than 65 years,
alanine aminotransferase (ALT) more than 42 U/l (irrespective of sex), positive tests for HBsAg/IgG anti-HBc/
anti-hepatitis C virus, clinical evidence of heart disease,
presence of active implantable medical devices, pregnancy, and alcohol drinking (> 20 g/day). All individuals
underwent ultrasound evaluation of the liver in search of
hepatic steatosis performed by an experienced abdominal
radiologist (R.E.) using a 15-MHz probe (Logiq P6 pro;
GE Healthcare, Berlin, Germany). First, a total of 40
individuals were excluded because of the presence of
steatosis on ultrasound. The mean (SD), median (minimummaximum), and 5th and 95th percentile values of
CAP values in the 40 individuals with steatosis on
ultrasound were 285.5 (48.59), 290.5 (174.0 367.0),

Final study group

(n = 102)

Flowchart of the cohort selection.

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1332 European Journal of Gastroenterology & Hepatology 2013, Vol 25 No 11

diastolic blood pressure, respectively. Routine blood

chemistry analyses were carried out at the central
laboratory of clinical chemistry of our institute. The
Ethics Committee of the Marmara University School of
Medicine approved this study and all participants
provided written informed consent before participation.
Liver stiffness measurement and determination
of controlled attenuation parameter

A single operator (Y.Y.) performed all Fibroscan examinations according to the manufacturers protocols. With the
patient lying in the dorsal decubitus position, the tip of
the transducer probe was placed on the skin between the
ribs over the right lobe of the liver. LSM assessment was
performed on a Fibroscan 502 touch (Echosens SA) using
the M probe according to the manufacturers instructions.
The examination was performed on the right lobe of
the liver through the intercostal space. After the area
of measurement was located, the examiner pressed the
button of the probe to start the acquisition. The
measurement depth was between 25 and 65 mm [26].
A reliable LSM result was defined as at least 10 valid shots,
a success rate of at least 60%, and interquartile range less
than 30% of the median LSM value [26]. Results were
considered unreliable if these criteria were not fulfilled.
CAP examinations with no successful measurements after
at least 10 attempts were deemed as failures. As an
indicator of variability, the ratio of the interquartile range of
CAP to the median was calculated. The final CAP value,
which ranges from 100 to 400 dB/m [2123], represents the
median of individual measurements.
Data analysis

The KolmogorovSmirnov test was carried out for all

continuous variables to define the presence of normality.
Gaussian variables are expressed as meanSD, skewed
data are reported as medians and interquartile ranges, and
categorical variables are expressed as counts. Skewed
variables were logarithmically transformed to improve
normality before analysis and then back-transformed to
their natural units for presentation in the text and tables.
Correlations among the study variables were tested using
Spearmans correlation coefficient. Multivariable linear
regression analysis with a stepwise forward selection
procedure was used to identify the independent predictors of CAP; the covariates included in the multivariable model were all of the variables listed in Table 1.
All statistical analyses were carried out using SPSS
version 14.0 for Windows (SPSS Inc., Chicago, Illinois,
USA). A value of P less than 0.05 (two-sided) was
considered statistically significant.

Results
The inclusion and exclusion criteria were fulfilled in 102
individuals (Table 1). The results of LSM and CAP
assessment are presented in Table 2. The mean (SD),
median (minimum maximum), and 5th and 95th

Table 1

General characteristics of the study participants

Participants (n = 102)

Sex (male/female)
Age (years)
BMI (kg/m2)
Waist circumference (cm)
Hip circumference (cm)
Systolic blood pressure (mmHg)
Diastolic blood pressure (mmHg)
Fasting plasma glucose (mg/dl)
AST (U/l)
ALT (U/l)
Total cholesterol (mg/dl)
HDL cholesterol (mg/dl)
LDL cholesterol (mg/dl)
Triglycerides (mg/dl)
Number of criteria for the MS (0/1/2)

64/38
359
23.33.5
8110
947
11711
748
858
196
167
18634
4117
12831
68 (41100)
43/48/11

Data are presented as means and SD, counts, or medians and interquartile
ranges, as appropriate.
ALT, alanine aminotransferase; AST, aspartate aminotransferase; HDL, highdensity lipoprotein; LDL, low-density lipoprotein; MS, metabolic syndrome.

Table 2

Fibroscan parameters of the study participants

Participants (n = 102)

LSM (kPa)
Valid shots (n)
Success rate (%)
Interquartile range
Interquartile range
CAP (dB/m)
Interquartile range
Interquartile range

LSM
LSM/median
CAP
CAP/median

5.451.90
11.81.7
91.411.7
0.950.58
16.97.3
206.9948.12
45.3225.30
23.3815.21

CAP, controlled attenuation parameter; LSM, liver stiffness measurement.

percentile values of LSM values in this cohort of 102

individuals were 5.45 (1.90), 5.0 (2.3 11.9), 3.1 and
9.4 kPa, respectively. Therefore, the normal range of LSM
in our population was 3.1 9.4 kPa. There was no
correlation between LSM and all of the variables listed
in Table 1 in our patients (data not shown).
The mean (SD), median (minimum maximum), and
5th and 95th percentile values of CAP values in this
cohort of 102 individuals were 206.99 (48.12), 210.5
(100.0 314.0), 113.4 and 280.2 dB/m, respectively.
Therefore, the normal range of CAP in our population
was 113.4280.2 dB/m. In univariate correlation analyses,
the CAP values were significantly associated with age
(r = 0.25, P < 0.05), BMI (r = 0.47, P < 0.001), waist
circumference (r = 0.46, P < 0.001), hip circumference
(r = 0.40, P < 0.001), systolic blood pressure (r = 0.27,
P < 0.01), diastolic blood pressure (r = 0.21, P < 0.05),
serum ALT levels (r = 0.26, P < 0.01, Fig. 2), and the
number of metabolic syndrome criteria (r = 0.33, P < 0.01).
In multivariable analysis, CAP was independently associated with BMI (b = 0.39, t = 3.5, P < 0.001) and the
number of metabolic syndrome criteria (b = 0.24, t = 2.1,
P < 0.05). We estimated the number of individuals with
undiagnosed steatosis who could be detected using
different cut-off points for CAP according to previous

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Steatosis on transient elastagraphy Yilmaz et al. 1333

Fig. 2

350

CAP (dB/m)

300

250

200

150

100
5

10

15

20
25
ALT (U/l)

30

35

40

Scatterplot and regression line showing a significant positive relation

between alanine aminotransferase levels and controlled attenuation
parameter (CAP) in the study participants.

studies carried out in patients with chronic hepatitis

C [20], patients with chronic liver disease from various
causes [18], and overweight patients with chronic liver
disease and a BMI of at least 28 kg/m2 [21]. Using the
previously identified cut-offs of 222 dB/m [20], 238 dB/m
[18], and 283 dB/m [21] of CAP for the presence of
significant steatosis (Z 10% of affected hepatocytes), 39
(38.2%), 23 (22.5%), and five (4.9%) patients of the 102
had at least 10% steatosis despite normal liver findings on
ultrasound. Compared with the 63 patients with a CAP
less than 222 dB/m, the 39 patients who had a CAP above
the cut-off of 222 dB/m had a significantly higher BMI
(22.73.5 vs. 25.63.6 kg/m2, respectively, P < 0.001)
and a greater number of metabolic syndrome criteria
(1.20.8 vs. 2.10.6, respectively, P < 0.05).

Discussion
Despite the increasing popularity of CAP to explore
hepatic steatosis [1823], this index has not been
evaluated as a screening procedure in apparently healthy
individuals. A significant finding in this report is the
validation of CAP as a reliable diagnostic method to
screen the general population for steatosis. On the basis
of the presence of a CAP value more than 283 dB/m [21],
we could indeed detect previously unknown liver
steatosis in at least 4.9% of the study participants with
normal findings on ultrasound.
Currently, the reference standard for hepatic steatosis
assessment is the histopathologic analysis of a liver
biopsy [1]. Unfortunately, this is an invasive and costly
procedure with the potential of complications [27]. In
addition, liver biopsy is also prone to sampling error and
interobserver variability [28]. Consequently, there is an
increasing demand for noninvasive tests to assess liver

steatosis because of the reluctance of patients to undergo

liver biopsy. Remarkably, the number of patients at risk
for NAFLD is so high that liver biopsy is not a practical
and efficient tool for screening purposes at the population
level [29]. Tools useful in screening for hepatic steatosis
are being actively sought, and CAP has been recently
suggested to be very efficient in the detection of even
low-grade steatosis [1823]. Besides being noninvasive,
quantitative, nonionizing, and inexpensive, CAP measurements are easy to perform, and machine and operator
independent [2123]. Importantly, CAP does not require
corrections to be made for gain, frequency, focusing, or
beam diffraction. Importantly, steatosis is the only
histological parameter significantly related to CAP that
is not influenced by fibrosis or inflammation. As CAP
measures on Fibroscan have been developed only recently,
the key issue of cut-off CAP values for the diagnosis of
liver steatosis has not been resolved as yet. For this
reason, the sensitivity and specificity will vary according
to the threshold value selected [18,20,21]. Naturally, one
could trade off sensitivity for better specificity and vice
versa by setting a different threshold value. Using the
previously identified cut-offs of 222, 238, and 283 dB/m
for CAP [18,20,21], the percentage of patients who had at
least 10% steatosis despite normal liver findings on
ultrasound varied between 4.9 and 38.2% in this study.
The suboptimal performance of ultrasound in the
detection of steatosis is not surprising because this
procedure is highly operator and machine dependent [16].
Because of the variability in cut-off values, cut-off ranges
rather than a single cut-off value should be used. For
example, in patients with CAP less than 222 dB/m, there
is likely minimal or no steatosis, whereas this condition is
likely in patients with CAP more than 283 dB/m. In the
current study, there was a positive and independent
association of CAP between both BMI and the number of
metabolic syndrome criteria, two of the main risk factors
for the development of NAFLD. As transient elastography
is a relatively new technology, the long-term prognostic
application of CAP is becoming available only now.
Our study has some limitations. We included a relatively
small convenience sample of 102 Turkish individuals in
apparently good health. Therefore, extrapolations and
generalizations of our findings to other populations
should take into account the specific age, sex, and ethnic
characteristics of the samples being compared. For this
reason, the external validation of our findings is warranted.
As it was not a main objective of our study, we did not
compare the diagnostic performance of different imaging
modalities for the detection of hepatic steatosis. Because
our study was focused on apparently healthy individuals,
the histological confirmation of hepatic steatosis on liver
biopsies was unfeasible for ethical reasons. Finally, this
study used CAP measurements at a single time point.
Given that all of the participants were without overt liver
disease, the reproducibility of transient elastography may

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

1334 European Journal of Gastroenterology & Hepatology 2013, Vol 25 No 11

have been compromised. Serial or repeated CAP measurements are likely to be more accurate.

10

Although additional validation is needed, these promising

results support the use of the CAP as a noninvasive,
immediate, and screening-friendly method to detect
steatosis in the general population. The use of CAP may
identify those individuals who are at a higher risk of
subsequently developing NAFLD, and therefore merit
closer follow-up. Future longitudinal studies are needed to
determine whether CAP values higher than 222 dB/m are
associated with a significantly increased risk of biopsyproven NAFLD. Importantly, our results may lead to further
studies on the potential usefulness of CAP for selecting
living-related donor livers in a transplantation setting. In
this respect, the presence of macrovesicular steatosis is
associated with an increased risk of graft loss [30]. Because
it has been reported that half of the living-related liver
donors appearing absolutely healthy on ultrasound had
biopsies with abnormal pathology results [31], it can be
speculated that CAP assessment may be clinically useful for
transplant purposes. Finally, future studies should compare the cost-effectiveness of CAP screening with other
screening procedures for the detection of hepatic steatosis.

11

Acknowledgements
This study was financially supported by the Institute of
Gastroenterology, Marmara University, Istanbul, Turkey.

12

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15
16

17

18

19

20

21

22

Conflicts of interest

23

There are no conflicts of interest.

24

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