Abdominal Ultrasound Findings of Tumor-Forming Hepatic Malignant Lymphoma
Abdominal Ultrasound Findings of Tumor-Forming Hepatic Malignant Lymphoma
Abdominal Ultrasound Findings of Tumor-Forming Hepatic Malignant Lymphoma
E-Mail hirage @ m.ehime-u.ac.jp
A malignant lymphoma (ML) is known to be derived tissue [11], n = 2, Hodgkin’s lymphoma, n = 2, B-cell lym-
from lymphatic tissue. Evaluations of abdominal ultraso- phoma [details unknown], n = 2, DLBCL + methotrexate-
nography (US) findings of primary and secondary tu- associated lymphoproliferative disorders [MTX-LPD],
mor-forming hepatic ML (HML) tumors have not been n = 1, T-cell lymphoma + MTX-LPD, n = 1, adult T-cell
adequately reported. It is generally considered that an lymphoma, n = 1, MTX-LPD [12], n = 1). The median tu-
HML is revealed as a homogeneous hypo-echoic lesion mor size was 26 mm (interquartile range 17–50 mm). Al-
[1–3] that often includes a portal or hepatic vein inside of though all lesions were revealed as hypo-echoic with con-
the tumor without invasion (penetrating sign) [4, 5] in ventional US, the internal echo was revealed as heteroge-
conventional US findings. However, a small number of neous in 10 and homogeneous in 15. The border of the
patients with HML shows that there is a lack of determin- tumor was unclear in 11. Inside the tumor, penetrating
istic findings in US and contrast-enhanced US (CEUS) sign was detected in 9 patients. Dilatation of the distal in-
examinations. As a result, differential diagnosis from oth- trahepatic bile duct by the tumor was observed in 4.
er types of malignant hepatic tumors, such as hepatocel- When the cohort was divided into 2 groups according
lular carcinoma (HCC) [6, 7] and cholangiocellular car- to tumor diameter (<30 mm, small group, n = 14; ≥30
cinoma (CCC) [8], is difficult in some cases using US. In mm, large group, n = 11), the tumors of 10 patients in the
the present study, we elucidated US and CEUS findings large group were revealed as a heterogeneous hypo-echo-
obtained in patients with HML. ic tumor, 9 had an unclear boundary, and 8 had penetrat-
ing sign. Dilatation of the distal intrahepatic bile duct by
the tumor was observed in only 4 of the large group cases.
Materials and Methods On the contrary, all in the small group were revealed as
homogeneous hypo-echoic tumors, while 12 had a clear
We enrolled 25 patients diagnosed with HML based on patho-
boundary and only 1 had penetrating sign.
logical findings, obtained from examinations performed at our
hospitals from January 2006 to March 2017. The definition of pri- Eighteen patients were examined with CEUS. In the ar-
mary HML proposed by Ohsawa et al. [9] was used in this study. terial phase, 13 showed a homogeneous enhancement, 2 a
All underwent US examinations, while CEUS was performed in 18 basket pattern, and 2 an avascular area, while 1 had a spoke-
(72%) with HI VISION Preirus (probe: EUP-C715, 3.0 MHz, MI wheel pattern in the early vascular phase. In addition, 16
0.2; Hitachi, Tokyo, Japan) or Logic E9 (probe: C1–6-D, 3.4 MHz,
showed a washout pattern in the portal phase and 2 were
MI 0.25, GE Healthcare Medical Systems, Milwaukee, WI, USA,
Perflubutane (Sonazoid®, Daiichi Sankyo Co. Ltd., Tokyo, Japan) revealed as iso-vascular. All were shown as a defect in the
(0.5 mL/kg of body weight) was injected as the contrast agent for post-vascular phase. The 18 patients who were examined
each CEUS examination. The arterial phase of CEUS imaging was with CEUS were divided into 2 groups based on tumor di-
identified at 10–60 s after, and the post-vascular phase at 10 min ameter (<30 mm, small group, n = 11; ≥30 mm, large group,
after the injection. The portal phase of CEUS imaging was identi-
n = 7). Among those patients in the large group in whom
fied at 1–2 min after perflubutane injection. Findings of US and
CEUS were evaluated in a retrospective manner. When the anti- CEUS was performed, 3 showed homogeneous enhance-
body for hepatitis C virus (HCV)/HCV-RNA or hepatitis B surface ment, 2 had avascular area, 1 showed a basket pattern, 1 had
antigen was detected, the patients were determined to have a a spoke-wheel pattern in the early vascular phase, and 5
chronic HCV or hepatitis B virus (HBV) infection. showed a washout pattern in the portal phase, while all were
Fischer’s exact test was used for comparisons with the EZR
revealed as a defect in the post-vascular phase. Among the
package [10] using the R program. The study protocol was ap-
proved by the Institutional Ethics Committee of Ehime Prefec- 11 patients in the small group, 10 showed homogeneous
tural Central Hospital (No. 28–52). enhancements and 1 a basket pattern in the early vascular
phase, while all had a washout pattern in the portal phase
and were revealed as a defect in the post-vascular phase.
The clinical characteristics of patients with primary
Results (n = 7) and secondary (n = 18) HML are shown in Table 2.
In the primary HML group (n = 7), 5 had a heterogeneous
The clinical characteristics of the present cohort are hypo-echoic tumor with an unclear boundary and 5 had a
shown in Table 1 (median age 70 years, interquartile range large-sized tumor (≥30 mm). All were examined with
58–81 years; 15 males, 10 females; 7 primary, 18 second- CEUS. Images obtained in the early vascular phase showed
ary; 6 HCV, 5 HBV, 14 no liver disease; diffuse large B-cell various features, including 5 tumors with a washout pat-
lymphoma [DLBCL], n = 13, DLBCL + mucosa-associat- tern in the portal phase, which were revealed as a defect in
ed lymphoid tissue, n = 2, mucosa-associated lymphoid the post-vascular phase. Among those in the secondary
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500
Case Age, Primary/ HBV/ Conventional abdominal ultrasonography CEUS Pathological
Number years/ secondary HCV diagnosis
sex tumor internal echo boundary penetrating dilatation of early portal post-
size, mm sign intrahepatic vascular phase vascular
bile duct by phase phase
tumor
1 64/M Primary –/– 100 Hetero/hypo Unclear + + Hypervascular Iso-vascular Defect DLBCL
basket pattern
chaotic vessels
2 71/F Primary –/– 58 Hetero/hypo Unclear – – Iso-vascular Washout Defect DLBCL +
with avascular MTX-LPD
area
3 61/M Primary +/– 54 Hetero/hypo Unclear + – Hypervascular Washout Defect MALT
10 89/F Secondary –/– 32 Hetero/hypo Unclear + + NE DLBCL
Kitahata et al.
11 83/M Primary –/+ 30 Hetero/hypo Unclear + – Hypervascular Washout Defect DLBCL + MALT
homogeneous-
enhancement
12 86/M Secondary –/+ 27 Homo/hypo Clear – – Hypervascular Washout Defect DLBCL
homogeneous-
enhancement
13 54/F Secondary –/– 26 Homo/hypo Clear – – NE T-cell
lymphoma +
MTX-LPD
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Table 1. (continued)
US Findings of HML
14 78/F Secondary –/– 26 Homo/hypo Unclear + – Hypervascular Washout Defect MTX-LPD
homogeneous-
enhancement
15 58/M Primary –/– 22 Homo/hypo Clear – – Hypervascular Washout Defect MALT
homogeneous-
enhancement
16 43/M Secondary –/– 20 Homo/hypo Unclear – – NE DLBCL
17 80/F Secondary –/+ 19 Homo/hypo Clear – – Hypervascular Washout Defect Hodgkin’s
homogeneous- lymphoma
enhancement
18 70/F Secondary +/– 17 Homo/hypo Clear – – Iso-vascular Washout Defect DLBCL
homogeneous-
enhancement
19 81/F Secondary –/+ 17 Homo/hypo Clear – – Hypervascular Washout Defect DLBCL
homogeneous-
enhancement
20 87/M Secondary –/– 15 Homo/hypo Clear – – Iso-vascular Washout Defect DLBCL
homogeneous-
enhancement
21 73/F Secondary +/– 15 Homo/hypo Clear – – Iso-vascular Washout Defect DLBCL
homogeneous-
CEUS, contrast-enhanced ultrasonography; hetero, heterogeneous; homo, homogeneous; hypo, hypo-echoic; NE, not examined; DLBCL, diffuse large B-cell lymphoma;
MTX-LPD, methotrexate-associated lymphoproliferative disorders; MALT, mucosa-associated lymphoid tissue.
501
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a b
Fig. 1. Case 1: an 89-year-old Japanese female with diffuse large B- rowhead) was detected inside of the tumor and dilatation of the
cell lymphoma. A heterogeneous hypo-echoic nodule with an un- intrahepatic bile duct (arrow) by the tumor was observed (b).
clear boundary (black arrowhead) was detected in the second seg- Pathologically, the tumor was diagnosed as secondary hepatic ma-
ment of the liver (32 mm in diameter) by conventional abdominal lignant lymphoma (diffuse large B-cell lymphoma).
ultrasonography (US; a). Penetrating sign (hepatic vein: white ar-
HML group (n = 18), 13 had a homogeneous hypo-echoic Table 2. Conventional ultrasonography findings of primary and
tumor and 12 showed a clear boundary. In addition, a secondary tumor-forming hepatic malignant lymphoma
small-sized tumor (<30 mm) was found in 12 of these cas-
<30 mm ≥30 mm
es. CEUS was performed in 11 of the patients in the sec-
ondary HML group. Of those, 10 showed to be enhanced homo/ hetero/ homo/ hetero/
homogeneously in the early vascular phase, while all hypo hypo hypo hypo
showed a washout pattern in the portal phase and were Primary HML (n = 7) 02 0 0 5
revealed as a defect in the post-vascular phase. In both pri- Secondary HML (n = 18) 12 0 1 5
mary and secondary tumor-forming HMLs, there were
similar tendencies found in findings obtained with US and HML, hepatic malignant lymphoma; hetero, heterogeneous;
homo, homogeneous; hypo, hypo-echoic.
CEUS. Although the percentage of large-sized tumors was
greater in the primary cases, the difference was not sig-
nificant (5 of 7 (71.4%) vs. 6 of 18 (33.3%); p = 0.177).
DOI: 10.1159/000480138
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LOQIE
E9
a b
LOQIE
E9
c d
Fig. 2. Case 2: a 73-year-old Japanese female with diffuse large B- flubutane (CEUS), homogeneous enhancement in the early vascu-
cell lymphoma. A hepatic tumor (15 mm in diameter) was revealed lar phase (b) and a washout pattern in the portal phase (c) were
as a homogeneous hypo-echoic nodule with a clear boundary in observed, respectively. In the post-vascular phase of CEUS, the
the fifth segment of the liver by conventional B-mode of abdomi- tumor was revealed as a defect (d).
nal ultrasonography (US; a). In contrast-enhanced US with per-
Discussion ly 50–60% of autopsy cases with that tumor [16, 17]. Sec-
ondary HML has been reported to often progress from
ML is known as a malignant tumor that is derived from ML and the diffuse invasive type is most frequent [18].
lymphatic tissue, while it has been noted that HML com- It is considered that US findings of both primary and
prise approximately 8% of focal hepatic lesions [13]. A secondary tumor-forming HML have not been adequate-
primary HML has been reported to be a very rare malig- ly evaluated. Although a needle biopsy procedure for ML
nancy, representing 0.41–1% of extra-nodal lymphomas has a high rate for accurate diagnosis (85%) [19], differ-
[14–16]. On the contrary, it is well known that ML shows ential diagnosis including other malignant hepatic tu-
frequent invasion, as it has been reported in approximate- mors (e.g., HCC, CCC) can be difficult in some cases of
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