The British Journal of Radiology, 78 (2005), 189–197 E 2005 The British Institute of Radiology

DOI: 10.1259/bjr/75208448

Ultrasound evaluation of the fibrosis stage in chronic liver

disease by the simultaneous use of low and high frequency
probes
1
T NISHIURA, RMS, 1H WATANABE, RMS, 1,2M ITO, MD, 3Y MATSUOKA, MD, 4K YANO, MD,
4
M DAIKOKU, MD, 4H YATSUHASHI, MD, 4K DOHMEN, MD, FACP, SJSUM and
4
H ISHIBASHI, MD, FACP, SJSUM
1
Clinical Laboratory, 2Department of Pathology, 3Deartment of Radiology and 4Clinical Research Centre, NHO National
Nagasaki Medical Centre, Omura, Nagasaki, 856-8562 Japan

Abstract. A liver biopsy is currently considered the definitive diagnostic modality for establishing the severity of
hepatic fibrosis. We analysed the diagnostic sensitivity and accuracy of ultrasound (US) using both low
frequency and high frequency probes as a repeatable, inexpensive, and reliable method to determine the fibrosis
stage in chronic liver disease and then compared our results with the histological findings. A total of 103
patients with chronic liver disease (60 males and 43 females, average age 51 years old) who had undergone both
a liver biopsy and US with 2–5 MHz frequency and 5–12 MHz frequency probes were prospectively evaluated
in this study. An US scoring system using both the low frequency and high frequency probes was performed by
evaluating the edge, surface and parenchymal texture of the liver. Each score was obtained by evaluating three
parameters; the bluntness of the liver edge, the irregularity of the surface and the coarseness of the parenchymal
texture were evaluated and then compared with the histological findings. The US scores of the liver edge (rs:
0.6668), liver surface (rs: 0.9007) and liver parenchymal texture (rs: 0.8853) correlated significantly with the
fibrosis stage obtained based on the biopsy findings. The accumulated US scores of these three parameters,
however, was found to be the most reliable indicator (rs: 0.9524). Patients with an accumulated score of 6.5 or
more were all found to have fibrosis stage 4 in which the accuracy of our scoring system for correctly predicting
cirrhosis was found to be 100% sensitive. When an accumulated US score of 3 was interpreted to indicate mild
fibrosis (a fibrosis score of 0 or 1), all 42 patients with stage 0 or 1 fibrosis were found to have an accumulated
US score of 3 or less (a probability of 100%) and 42 of 53 patients with a score of 3 or less were found to have
stage 0 or 1 fibrosis (specificity of 79.2%). An ultrasound evaluation of the liver fibrosis stage based on the
scoring system using both low and high frequency probes was found to be a reliable and effective alternative to
the histological staging in chronic liver diseases.

The liver fibrosis stage in patients with chronic liver
diseases due to an infection with hepatitis B virus (HBV)
or C virus (HCV) is a pivotal factor regarding both the
therapeutic options and for predicting the prognosis. A
liver biopsy is considered to be the gold standard for diag-
nosing the liver fibrosis stage and predicting the outcome
of the diseases. Although a percutaneous liver biopsy is
relatively safe, it is still associated with a risk of com-
plications, patient discomfort and a high cost. In addition,
liver biopsy examinations may lead to false negative results
due to inadequate liver tissue sampling. Therefore, there is
a need to develop a simple, reliable and non-invasive
modality in order to assess the liver fibrosis stage [1].
Ultrasound (US) is a non-invasive, inexpensive and
repeatable modality and has been used as the most
important and valuable diagnostic tool for detecting
hepatocellular carcinoma (HCC) during the follow-up of
patients with viral hepatitis [2, 3]. US is also used for
monitoring the response of HCC to treatment.
Received 22 July 2003 and in final form 31 August 2004, accepted 5
October 2004.
Address correspondence to Dr Koji Yano, Clinical Research Centre,
NHO National Nagasaki Medical Centre, Kubara 2-1001-1 Omura,
Nagasaki 856-8562 Japan.
An ultrasound evaluation of the liver fibrosis stage of
chronic liver disease has been performed by assessing
various ultrasound factors such as the liver size, the
bluntness of the liver edge, the coarseness of the liver
parenchyma, nodularity of the liver surface, the size of the
lymph nodes around the hepatic artery, the irregularity
and narrowness of the inferior vena cava, portal vein
velocity or spleen size [1, 4–8]. However, the conventional
definition of the fibrosis stage of the liver based on
evaluation of these ultrasound factors is imperfect and
lacks accuracy and reliability. Furthermore, these findings
also depend largely on the equipment used [8]. Indeed, a
few reports have demonstrated no consistent correlation
between the grey scale ultrasound findings and the
histological findings, thus claiming that grey scale US is
unreliable for grading and staging the degree of liver
damage [9]. However, recent advances in US technology
have improved the diagnostic accuracy for fibrosis in
patients with chronic liver disease. Therefore, we carried
out a study to evaluate the accuracy of the liver fibrosis
stage by utilizing the techniques of advanced ultrasound
performance in 103 patients with chronic liver disease and
compared the results obtained with the histological
findings.

The British Journal of Radiology, March 2005 189


Patients and methods
Patients
This study was prospectively designed. 103 consecutive
patients, consisting of 60 males and 43 females with a
diagnosis of chronic liver disease including liver cirrhosis
at National Nagasaki Medical Centre between October
2001 and February 2003 were included. The mean age of
the patients was 51 years old, with a range of from 38
years to 75 years. The inclusion criteria were as follows: (a)
history of chronic liver disease, based on the detection of
persistently high levels of aminotransferase; (b) an absence
of clinical and/or biochemical signs of decompensated liver
diseases (jaundice, ascites or encephalopathy); and (c) no
previous histopathological diagnosis. Regarding the hepa-
titis virus, 22 patients were infected with HBV, 64 with
HCV, 5 with both HBV and HCV and 12 with neither
HBV nor HCV. Both ultrasound and histological exam-
ination obtained based on a liver biopsy were performed
for all patients.
US system
The patients were studied ultrasonically using a real-
time apparatus (HDI 5000 Sono CT, ATL, USA) with a
2–5 MHz convex array transducer C5–2 (low frequency
probe) and a 5–12 MHz convex array transducer L12–5
(high frequency probe).
US findings and the scoring system (Table 1)
The US examination was performed within an interval
of no more than 15 days prior to the biopsy examination.
The US examiners (TN, HW) were unaware of the clinical
details of the patients, and the US findings were
interpreted by two specialists (KY, HI) who had no
knowledge of either the biochemical or biopsy results. The
ultrasound examinations were recorded on static B-mode
imaging. The US examiners were both certified by the
Japan Society of Ultrasonics in Medicine. The US score
was determined from the right and left lobes and the
average score for each parameter was calculated as
follows: (1) liver edge (Figure 1): score 0 for sharp;
score 1 for mildly blunted; score 2 for blunted; (2) liver
surface (Figure 2): score 0 for smooth; score 1 for mildly
irregular; score 2 for irregular; score 3 for highly irregular;
and (3) liver parenchymal texture (Figure 3) [5, 10]: score 0
for fine; score 1 for mildly coarse; score 2 for coarse; score
3 for highly coarse. A score of 0 was given when no
abnormality was observed by a high frequency probe,
score 1 was given when a mild abnormality was detected
by a high frequency probe while it was undetected by the
low frequency probe, a score of 2 was given when a
moderate abnormality was detected by the low frequency
probe, and a score of 3 was given when a severe
abnormality was detected by the low frequency probe. A
Table 1. Findings for the ultrasound features of the edge, surface and parenchymal texture of the liver
Score 0 Score 1
Edge sharp mildly blunted edge
Surface smooth mildly irregular
Parenchymal texture fine mildly coarse
190
T Nishiura, H Watanabe, M Ito et al
score of 2 was given for a blunted edge and a score 3 for
severe irregular surface or a highly coarse texture when
these characteristics were clearly confirmed by the low
frequency probe. In cases in which three parameters such
as the edge, surface and parenchymal texture could not be
determined to be either mild or severe using a low
frequency probe, then the high frequency probe was used
to determine whether they were mild or severe. The high
frequency probe was used to obtain a score 0 or 1 because
the sensitivity obtained by the high frequency probe was
superior to the one by the low frequency probe regarding
mildly abnormal changes such as a score 0 or 1.
Conversely, regarding such advanced changes as a score
of 2 or 3, the low frequency probe was more useful
because the probability obtained by the low frequency
probe was superior to that by the high frequency probe.
As a result, the fibrosis stage predicted from the accumu-
lated scores of the liver edge, surface and parenchymal
texture by US were considerably more reliable than the
individual scores of these three parameters when they were
compared with the histological findings.
Histological findings
Liver biopsy specimens were obtained from the anterior
segment of the right lobe in each patient, using a 16-gauge
Sonopsy-C1 biopsy needle (Hakko Co., Tokyo, Japan).
All of the histological slides were reviewed by an
experienced pathologist without any knowledge of the
clinical details or the US findings. The New Inuyama
scoring system for chronic hepatitis was proposed by the
Japanese Liver Study Group in 1994 [11], which is similar
to the classification of chronic hepatitis determined by the
USA-European Liver Study Group [12]. The New
Inuyama scoring system was used to assess the fibrosis
stage as follows; score 0: no fibrosis, score 1: fibrous portal
expansion, score 2: bridging fibrosis, score 3: bridging
fibrosis with lobular degeneration, and score 4: cirrhosis.
Statistics
The Spearman’s correlation test was used to assess any
correlations between the liver fibrosis stage and the US
scoring system. The sensitivity, specificity and positive
predictive values of the US scoring system were calculated
and compared with the results of the liver fibrosis stages.
Results
US scoring system and fibrosis stage
The relationship between the liver edge and fibrosis
(Figure 4)
Of 11 patients with a sharp liver edge (edge score 0), 6
patients (55%) were found to have stage 0 fibrosis and 5
(45%) in stage 1 fibrosis. The liver edge score of 34 patients
Score 2 Score 3
blunted edge
irregular highly irregular
coarse highly coarse
The British Journal of Radiology, March 2005
US findings for chronic liver disease
(a)
(c)
in an early fibrosis stage (stage 1) showed various results; 5
patients had a score of 0, 6 a score 0.5, 9 a score of 1, 5 a
score of 1.5 and 9 a score of 2. On the other hand, the
patients with stage 2, 3 and 4 fibrosis correlated well with
the edge score and were categorized into a blunted edge
(score 2); 26 of 26 patients with stage 2 fibrosis, 12 of 13
patients with stage 3 fibrosis, 22 of 22 patients with stage 4
fibrosis. The liver edge and the fibrosis score thus showed
a statistically significant correlation (rs: 0.6668).
The relationship between the liver surface and fibrosis
(Figure 5)
Eight patients with stage 0 fibrosis were all put into the
smooth liver surface group (surface score 0), and 34
patients with the fibrosis stage 1 were all found to have a
The British Journal of Radiology, March 2005
(b)
Figure 1. The ultrasound features of the liver edge; (a) a sharp
edge with a high frequency probe, (b) a mildly blunted edge
with a high frequency probe, and (c) a blunted edge with a
low frequency probe.
score of 1 or less. 26 patients with the fibrosis stage 2 had
different results regarding the surface score, i.e. 3 patients
had a surface score of 0, 7 a score of 0.5, 9 a score of 1, 4 a
score of 1.5 and 3 a score of 2, respectively. 12 of 13
patients with stage 3 fibrosis were found to have a surface
score of either 1.5 or 2. All 22 patients with the stage 4
fibrosis were found to have a surface score of 2 or more.
The liver surface score and the fibrosis stage showed a
statistically significant correlation (rs: 0.9007).
The relationship between liver parenchymal texture and
fibrosis (Figure 6)
Eight patients with stage 0 fibrosis were all found to
have a fine liver parenchymal texture (parenchymal score
0), and 29 of 34 patients with stage 1 fibrosis were found
191

(a)
(c)
Figure 2. The ultrasound features of the liver surface; (a) a smooth surface with a high frequency probe, (b) a mildly irregular sur-
face with a high frequency probe, (c) an irregular surface with a low frequency probe, and (d) a highly irregular surface with a low
frequency probe.
to have a score of 0. Of 26 patients with stage 2 fibrosis, 11
had a score of 0, 14 a score of 1 and 1 a score of 2. Five
and 6 patients of the 13 patients with stage 3 fibrosis had a
score of 1 and 2, respectively. All 22 patients with stage 4
fibrosis had a parenchymal score of 2 or more. The liver
parenchymal score and the fibrosis stage showed a
statistically significant correlation (rs: 0.8853).
Relationship between the fibrosis grade and the
accumulated scores of the liver edge, surface and
parenchymal texture (Figure 7)
The liver edge, surface and parenchymal texture scores
were all determined and compared with the histological
192
T Nishiura, H Watanabe, M Ito et al
(b)
(d)
fibrosis score. Of eight patients with fibrosis stage 0, six
patients were found to have a total score of 0 and while
two had a total score of 1. 34 patients with stage 1 fibrosis
had a total score 1.53 consisting of 2 patients with scores
of 0, 11 and a score of 0.5–1, 17 had a score of 1.5–2.0,
and 4 had a score of 2.5–3, respectively. 26 patients with
stage 2 fibrosis shifted to the progressive fibrosis stage,
such as 1 patient with a score of 1.5–2, 10 with a score of
2.5–3, 9 with a score of 3.5–4, and 6 with a score of 4.5–5,
respectively. Similarly, 13 patients with stage 3 fibrosis
shifted to a progressive fibrosis stage such as 1 patient with
a score of 3.5–4, 5 with a score of 4.5–5, and 7 with a score
of 5.5–6, respectively. Out of 22 patients with stage 4
fibrosis had a score of 6.5–7.0 and eleven had a score of
The British Journal of Radiology, March 2005
US findings for chronic liver disease

(a) (b)

(c) (d)

Figure 3. Scores for the ultrasound features of the liver parenchymal texture; (a) fine parenchymal texture with a high frequency
probe, (b) a mildly coarse parenchymal texture with a high frequency probe, (c) a coarse parenchymal texture with a low frequency
probe, and (d) a highly coarse parenchymal texture with a low frequency probe.

7–7.5, respectively. The fibrosis grade and the accumulated
scores of these three parameters were more significantly
correlated (positive predictive value, 0.9524) than the
correlations of each score alone.
Discussion
Chronic liver diseases with viral infection manifest
varying degrees of hepatic fibrosis ranging from no fibrosis
to cirrhosis. Yoshida et al revealed that the annual
incidence of hepatocellular carcinoma increased from
0.5% among patients with the stage F0 or F1 fibrosis to
7.9% among the patients with stage F4 fibrosis [13]. It has
thus become increasingly apparent that the fibrosis stage is
a key factor in defining the prognosis and management of
chronic liver diseases with a viral infection.
The gold standard in hepatology for the diagnosis of
the fibrosis stage has been a histological liver evaluation
based on specimens taken either by a needle biopsy or at
operation. Recently, non-invasive and reliable assessments
for monitoring chronic liver disease using the platelet

The British Journal of Radiology, March 2005 193

 T Nishiura, H Watanabe, M Ito et al

Figure 4. Relationship between the liver edge and fibrosis findings.

Figure 5. Relationship between the liver surface and fibrosis findings.

194 The British Journal of Radiology, March 2005

US findings for chronic liver disease

Figure 6. Relationship between the liver parenchymal texture and fibrosis findings.

Figure 7. Relationship between the accumulated ultrasound score and fibrosis score findings.

The British Journal of Radiology, March 2005 195


counts [14–16], aspartate aminotransferase (AST)/alanine
aminotransferase (ALT) ratio [15, 16], and serum hyalur-
onan and type III procollagen amino-terminal peptide [17]
have been developed. However, none of the currently
available tests or modalities can completely replace a
histological analysis. Previous studies have assessed several
methods for evaluating the fibrosis stage of chronic liver
disease using various US parameters. However, there have
so far been few studies concerning the accuracy in
detecting the signs of compensated cirrhosis by US [5,
18]. Gaiani et al [5] and Hung et al [19] proposed a
complex US scoring system using indices of the liver
surface, parenchymal echogenecity, the vessel pattern,
spleen size etc. to determine the fibrosis stage. In addition,
recent advances in ultrasound technology have now made
it possible to obtain more precise information about the
liver surface, edge and parenchymal texture [8]. Therefore,
we conducted this study to clarify whether the US scoring
system with a newly developed US equipment based on the
conventional parameters of the liver edge, surface and
parenchymal texture might obtain sufficiently accurate
results in comparison with the histological findings for
fibrosis obtained by a liver biopsy.
In this prospective study, among these parameters such
as the liver edge, liver surface and liver parenchymal
texture, the liver edge was not as specific for evaluating
liver fibrosis as the liver surface and parenchymal texture
in our study because a mildly blunted (score 1) or blunted
edge (score 2) was frequently found in the early fibrosis
stage (stage 1) (67.6%). On the other hand, the liver
surface and liver parenchymal texture obtained by US
showed a better correlation with the histological findings
(correlation coefficient of 0.9007 in the liver surface, and
0.8853 in the parenchymal texture).
With conventional US, the liver surface has been most
commonly utilized as a sole indicator for the diagnosis of
cirrhosis [5, 20–22]. However, numerous papers have
reported that the sole factor of the liver surface can not
sufficiently distinguish cirrhosis from chronic hepatitis.
Gaiani et al confirmed that the stage of cirrhosis may be
underestimated when based on a single specimen and
clarified that only two US variables, namely liver surface
nodularity and the portal vein mean flow velocity,
independently contributed to the diagnosis of cirrhosis
[5]. In our study, all seven patients with a highly irregular
surface were found to have cirrhosis (stage 4 fibrosis)
histologically. On the other hand, 15 of 22 patients (68.2%)
with cirrhosis were found to have an irregular surface
(score 2–2.5), not a highly irregular surface (score 3).
Indeed, the results of our study showed a significant
correlation between the ultrasound liver surface and the
histological fibrosis stage.
An irregular and nodular liver surface may be easily
assessed in patients with decompensated liver cirrhosis,
particularly in the case of ascites, and it has been observed
in 88% of unselected patients with cirrhosis [20]. Gaiani
et al reported the findings of a US scoring system, based
on the liver, spleen and portal vein features, which
identified cirrhosis in 82.2% of the cases [5]. In our
study, both the right and the left liver lobes were evaluated
for each factor, and the average score for each parameter
was calculated. Both the low frequency and the high
frequency probes were used to limit the subjective nature
of the assessment of the US findings of various degrees. In
196
T Nishiura, H Watanabe, M Ito et al
this prospective study, US was performed with the
simultaneous use of low frequency and high frequency
probes to determine the sensitivity and probability
according to the characteristics of ultrasound. Although
our study was limited on account of the relatively small
number of patients due to the strict inclusion criteria, 22
patients with an accumulated score of 6.5 or more were all
found to have a fibrosis score of 4. Therefore, our scoring
system for correctly predicting cirrhosis was found to be
100% sensitive. Furthermore, although the major draw-
back with US in comparison with the liver histology has
been considered to be the failure to detect mild fibrosis or
none at all, our scoring system thus provided relatively
accurate information about liver fibrosis. When the
accumulated US score of 3 was interpreted as mild fibrosis
(a fibrosis score of 0 or 1), all 42 patients with stage 0 or 1
fibrosis were categorized into an accumulated US score of
3 or less (a probability of 100%) and 42 of 53 patients with
a score of 3 or less were found to have stage 0 or 1 fibrosis
(specificity of 79.2%). In addition, the score proposed in
our study is easy to obtain and can be applied in every
ultrasound laboratory by utilizing regular commercially
available US equipment.
Evaluating the ultrasound pattern using either one or
two parameters becomes much more complex at the stage
of chronic liver disease than that of complete cirrhosis.
Our scoring system based on three parameters such as the
liver edge, surface and parenchymal texture was able to
accurately predict the fibrosis stage (correlation coefficient
of 0.9524), especially when distinguishing chronic hepatitis
from compensated liver cirrhosis. When an exclusion of
liver cirrhosis is requested, then US alone is therefore
considered to provide sufficient information based on this
scoring system. Furthermore, if a histological analysis can
not determine the fibrosis stage correctly due to fragmen-
tation or architectural distortion, then this ultrasound
diagnostic modality of fibrosis could replace a histological
diagnosis.
In conclusion, we demonstrated that our US scoring
system is clinically useful for differentiating patients who
have chronic liver disease with minimal or no fibrosis
from those with mild to severe fibrosis. These parameters
may also be useful for providing prognostic informa-
tion and also for determining the optimal therapeutic
options during the follow-up of patients with chronic
liver disease, especially in patients with chronic hepatitis C
or B, in order to predict the occurrence of HCC. In
addition, further study is called for to determine whether
or not the wider use of this scoring system could apply to
other forms of hepatic fibrosis such as those suffering from
long-term hepatotoxic disease, congenital diseases in
children and non-viral infective forms of chronic liver
disease in order to obtain an improved response to
therapy.
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