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Sonographic Appearances of Small Hepatic
Nodules without Tumor Stain on
Contrast-Enhanced Computed Tomography
and Angiography
Masahiko Iwasaki, MD,1 Jyunji Furuse, MD,1 Masahiro Yoshino, MD,1 Munemasa Ryu, MD,2
Noriyuki Moriyama, MD,3 Kiyoshi Mukai, MD4
1
Department of Internal Medicine, National Cancer Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa-shi,
Chiba 277, Japan
2
Department of Surgery, National Cancer Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa-shi,
Chiba 277, Japan
3
Department of Radiology, National Cancer Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa-shi,
Chiba 277, Japan
4
Pathology Division, National Cancer Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa-shi, Chiba 277, Japan
Received 11 October 1996; accepted 22 November 1997
ABSTRACT: Purpose. We report the sonographic appearances and pathologic findings for hepatic nodules
2 cm or smaller that were detected by sonography but
that did not produce a tumor stain on constrastenhanced helical CT or digital subtraction angiography.
Methods. Sixty-six nodules 2 cm or less were found
by sonography in 39 patients. Sonographically guided
needle biopsies were done on all lesions.
Results. Twenty-seven nodules were benign nodules, 9 were borderline lesions, and 30 were hepatocellular carcinomas. Benign nodules were significantly smaller than hepatocellular carcinomas (mean
size, 1.0 cm versus 1.4 cm, respectively; p <0.00001).
Nodules 1 cm or smaller were more likely to be diagnosed as benign nodules (68%) than as either of the
other types (32%; p = 0.01). A significantly greater percentage of hepatocellular carcinomas showed a heterogeneous pattern (64%) on sonography compared
with benign nodules (25%) and borderline lesions
(11%; p = 0.04). In nodules 1 cm or smaller, a homogeneous pattern (68%) was more common than a heterogeneous pattern (32%; p = 0.01).
Conclusions. The nature of small hepatic nodules
cannot be determined with sonography. Thus, biopsy
Correspondence to: M. Iwasaki, Department of Internal Medicine, Tanaka Nokyo Hospital, 110, Wakashiba, Kashiwa-shi,
Chiba 277, Japan.
© 1998 John Wiley & Sons, Inc.
VOL. 26, NO. 6, JULY/AUGUST 1998
CCC 0091-2751/98/060303-05
remains the only technique for obtaining a definitive
diagnosis. © 1998 John Wiley & Sons, Inc. J Clin Ultrasound 26:303–307, 1998.
Keywords: hepatic nodule; needle biopsy; hepatocellular carcinoma; ultrasonography; computed tomography; angiography
M
any studies have examined the ability of sonography, CT, and angiography to detect
small hepatocellular carcinomas (HCCs). 1–4
HCCs larger than 2 cm can usually be diagnosed
with contrast-enhanced CT or angiography because they show a definite tumor stain.1,5–8 In
patients with chronic viral liver diseases, some
hepatic nodules 2 cm or less can be detected by
sonography, but their nature is difficult to determine by contrast-enhanced CT or digital subtraction angiography (DSA) because they may not
show a tumor stain. Furthermore, hepatologists
who use sonography to monitor patients with
chronic viral liver diseases for the development of
HCC must determine the nature of any nodules
discovered. In this retrospective study, we reviewed the sonographic appearances and pathologic findings for small hepatic nodules that did
not show a tumor stain on contrast-enhanced CT
or DSA.
303
IWASAKI ET AL
PATIENTS AND METHODS
Patients
Between 1992 and 1995, 66 hepatic nodules 2 cm
or less that were detected by sonography but that
failed to produce a tumor stain on contrastenhanced CT or DSA were identified in 39 patients with chronic viral liver diseases. The patients were 46–77 years old (mean, 63 years);
there were 29 men and 10 women. The status of
liver dysfunction was classified as Child’s class A
in 21 patients, class B in 13 patients, and class C
in 5 patients. HCC had not been previously diagnosed in 19 patients. Eleven patients had previously been treated for HCC (7 patients by resection, 3 patients by percutaneous ethanol injection,
and 1 patient by transhepatic arterial embolization). In the remaining 9 patients, small nodules
were found during workup for HCC in another
hepatic segment, which had been diagnosed by
contrast-enhanced CT or DSA. The locations of
the 66 nodules identified by sonography were as
follows: 7 were in the lateral segment of the left
lobe, 9 were in the medial segment of the left lobe,
27 were in the anterior segment of the right lobe,
and 23 were in the posterior segment of the right
lobe. Serum levels of hepatitis B surface antigen
and hepatitis C virus antibody were measured by
enzyme immunoassay. Two patients tested positive for hepatitis B surface antigen, 35 patients
tested positive for hepatitis C virus antibody, and
2 patients tested positive for both.
contrast medium at a rate of 2–3 ml/second. Portal-phase images were obtained 5 minutes later.9
DSA was performed by selective catheterization of the hepatic artery and administration of
10–30 ml of contrast medium at a rate of 1–3 ml/
second.
Liver Biopsy
Percutaneous liver biopsies were performed under sonographic guidance using a Menghini-type
cutting needle (Sonopsy; Hakko, Tokyo, Japan).
At least 2 cores of liver tissue were obtained from
most patients. None of the nodules identified by
sonography had been treated before the biopsy.
Pathologic Diagnosis
All nodules were classified as benign nodules, borderline lesions, or HCCs. When cirrhotic or nonneoplastic liver tissue was obtained, the nodule
was designated benign. Nodules demonstrating
adenomatous hyperplasia or atypical adenomatous hyperplasia were designated borderline lesions.10 HCCs were assigned a histologic grade
based on the dominant grade found in the nodule.
Statistical Analysis
Student’s t-test and the chi-squared test were
used for statistical analyses. A p value less than
0.05 was considered significant.
RESULTS
Diagnostic Procedures
Both sonography and contrast-enhanced helical
CT were performed at regular intervals as followup in patients with chronic viral liver diseases.
Whenever a nodule was detected in the liver by
sonography, contrast-enhanced helical CT and
DSA were performed. A diagnosis of HCC was
made only when a nodule detected by sonography
showed a tumor stain on contrast-enhanced CT in
the arterial phase of enhancement or on DSA.
Sonography was performed with a Toshiba
SSA 270A ultrasound scanner (Toshiba Corp., Tokyo, Japan) with a 3.75-MHz probe. Identified
nodules were categorized by echogenicity (hyperechoic, isoechoic, or hypoechoic) and homogeneity
(homogeneous or heterogeneous).
Contrast-enhanced helical CT was performed
with a Toshiba X vision/real CT scanner (Toshiba
Corp.). Arterial-phase images were obtained 30
seconds after the administration of 100–120 ml of
304
Pathologic Findings
Pathology showed that 27 nodules (41%) were benign nodules, 9 (14%) were borderline lesions, and
30 (45%) were HCCs. Figure 1 shows the distribution of these 3 types by size. Benign nodules
were significantly smaller than HCCs (mean ±
standard deviation, 1.0 ± 0.3 cm versus 1.4 ± 0.4
cm, respectively; p < 0.00001). The mean size of
borderline lesions was 1.2 ± 0.3 cm. Of the 30
HCCs, 26 (87%) were well differentiated and 4
(13%) were moderately differentiated. The mean
sizes of the well versus moderately differentiated
HCCs were not significantly different. Nodules 1
cm or smaller were more likely to be benign nodules (68%) than either of the other types (32%; p
4 0.01) (Table 1). All patients in whom benign
nodules had been found were followed for at least
6 months, with no change in the sizes of any of the
nodules.
JOURNAL OF CLINICAL ULTRASOUND
SMALL HEPATIC NODULES
FIGURE 2. Sonogram showing a 1.0-cm, hypoechoic, homogeneous
nodule (arrow) that was found on biopsy to be benign.
FIGURE 1. Relationship between pathologic diagnosis and the diameter of hepatic nodules 2 cm or less detected by sonography but
without tumor stain on contrast-enhanced helical CT or digital subtraction angiography. Numbers at top are means ± standard deviations. HCC, hepatocellular carcinoma.
TABLE 1
Pathologic Diagnoses of Small Hepatic Nodules Detected
by Sonography
No. Nodules by Pathologic
Diagnosis (%)
Diameter of
Total
Hepatic Nodules Nodules Benign Nodule Borderline
ø1 cm
>1 but ø 2 cm
19
47
13 (68)*
14 (30)
1 (5)
8 (17)
HCC
5 (26)
25 (53)
Abbreviation: HCC, hepatocellular carcinoma.
*For lesions ø 1 cm, p = 0.01 for benign nodules versus other
diagnoses.
FIGURE 3. Sonogram showing a 0.7-cm, hypoechoic, homogeneous
nodule (arrow) that was found on biopsy to be a hepatocellular carcinoma.
Sonographic Findings
patic nodules 2 cm or less can be detected only
with sonography, and their nature cannot be confirmed by contrast-enhanced helical CT or DSA
because of the lack of tumor stain. In this study,
we investigated the nature of such nodules.
Sonoda et al11 reported that resected small
HCCs that had not been detected angiographically had the following pathologic characteristics:
absence of a fibrous capsule; well-differentiated
grade; replacement by a cancerous cell growth
pattern; and remnant portal tracts within the tumor. Because our specimens were obtained by
needle biopsy, similar histologic analysis was not
possible, but the majority (87%) of our small
HCCs were well differentiated. Similarly, Yoshimatsu et al12 reported that 8 of 22 lesions smaller
than 2 cm detected by sonography were not identified by conventional angiography or DSA but
that all 8 lesions were well-differentiated HCCs
(Edmondson-Steiner grade I or II). Previous stud-
Figures 2–4 show the sonographic appearances of
the various hepatic nodules. None of the nodules
were isoechoic, and no relationship was seen between the echogenicity and the pathologic diagnosis (Table 2). A significantly greater percentage
of HCCs showed a heterogeneous pattern (64%)
compared with benign nodules (25%) and borderline lesions (11%; p 4 0.04) (Table 2). Most nodules 1 cm or smaller had a homogeneous (68%)
rather than heterogeneous pattern (32%; p 4
0.01) (Table 3).
DISCUSSION
In previous studies, HCCs smaller than 2 cm frequently appeared as hypovascular masses on angiography.1,5,8 Recently, helical CT has increased
the detection rate for HCCs.9 However, some heVOL. 26, NO. 6, JULY/AUGUST 1998
305
IWASAKI ET AL
FIGURE 4. Sonogram showing a 2.0-cm lesion with a heterogeneous
echo pattern that was found on biopsy to be a hepatocellular carcinoma. The nodule has a central anechoic area (arrowhead) with a
mildly echogenic rim (arrow).
TABLE 2
Sonographic Appearances versus Pathologic Diagnoses of
Small Hepatic Nodules
nodules measuring less than 1 cm were more
likely to be diagnosed as benign nodules than as
HCCs. Our findings were similar, except that
small nodules that had a heterogeneous pattern
on sonography were more likely to be malignant
than benign. The use of color Doppler imaging in
the assessment of HCCs has been reported.17
However, color Doppler imaging was not used in
our study.
In conclusion, hepatic nodules 2 cm or less can
be detected by sonography, but their nature (benign or malignant) cannot be determined if they
do not show tumor staining on contrast-enhanced
helical CT or DSA. Thus, for sonographically detected small hepatic nodules, sonography-guided
percutaneous needle biopsy remains the only
technique for definitive diagnosis.
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No. Nodules by Pathologic
Diagnosis (%)
Sonographic
Findings
Echogenicity
Hyperechoic
Hypoechoic
Homogeneity
Homogeneous
Heterogeneous
Total
Nodules
Benign
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Borderline
HCC
29
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36
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7 (23)
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Abbreviation: HCC, hepatocellular carcinoma.
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TABLE 3
Sonographic Appearances of Small Hepatic Nodules
No. Nodules by Sonographic Appearance (%)
Echogenicity
Diameter of
Hepatic Nodules
ø1 cm
>1 but ø 2 cm
Homogeneity
Total
Nodules
Hyperechoic
Hypoechoic
Homogeneous
Heterogeneous
19
47
6 (32)
23 (49)
13 (68)
24 (51)
13 (68)*
17 (36)
6 (32)
30 (64)
*For lesions ø 1 cm, p = 0.01 for homogeneous versus heterogeneous appearance on sonography.
306
JOURNAL OF CLINICAL ULTRASOUND
SMALL HEPATIC NODULES
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VOL. 26, NO. 6, JULY/AUGUST 1998
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307
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