Abdominal Ultrasound Findings of Tumor-Forming Hepatic Malignant Lymphoma

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Original Paper

Dig Dis 2017;35:498–505


DOI: 10.1159/000480138

Abdominal Ultrasound Findings of


Tumor-Forming Hepatic Malignant
Lymphoma
Shogo Kitahata a Atsushi Hiraoka a Masatoshi Kudo b Taisei Murakami a
Marie Ochi a Hirofumi Izumoto a Hidetaro Ueki a Miho Kaneto a
Toshihiko Aibiki a Tomonari Okudaira a Hiroka Yamago a Yuji Miyamoto a
Ryuichiro Iwasaki a Hideomi Tomida a Kenichiro Mori a Masato Kishida a
Hideki Miyata a Eiji Tsubouchi a Masashi Hirooka c Yohei Koizumi c
Tomoyuki Ninomiya a Yoichi Hiasa b Kojiro Michitaka a
a
Gastroenterology Center, Ehime Prefectural Central Hospital, Matsuyama, b Kindai University School of Medicine,
Department of Gastroenterology and Hepatology, Osaka, and c Department of Gastroenterology and Metabology,
Ehime University Graduate School of Medicine, Toon, Japan

Keywords geneous hypo-echoic type (100%), with penetrating sign


Hepatic malignant lymphoma · Ultrasonography · observed in only 1 patient. Tumors in 11 patients in the
Contrast-enhanced ultrasonography · Perflubutane small group, examined with CEUS, showed homogeneous
enhancement in the early vascular phase (91%) and a
washout pattern in the portal phase (100%), and they were
Abstract revealed as defective in the post-vascular phase (100%). In
Aim/Background: Evaluations of abdominal ultrasonogra- the large group (≥30 mm; n = 11), tumors were revealed
phy (US) findings of primary and secondary tumor-forming as a heterogeneous hypo-echoic lesion in 10 (91%) and
hepatic malignant lymphoma (HML) have not been ade- penetrating sign was observed in 8 (73%). Dilatation of the
quately reported. In this study, we elucidated US and con- distal intrahepatic bile duct by the tumor was observed in
trast-enhanced US (CEUS) findings in patients with HML. 4 patients in the large group. In 7 large group patients ex-
Materials/Methods: From January 2006 to March 2017, 25 amined with CEUS, imaging findings in the early vascular
patients with HML were enrolled (primary 7, secondary 18), phase varied, with 5 (71%) showing a washout pattern in
each of whom was diagnosed pathologically. They were the portal phase and 5 (71%) revealed as defective in the
divided into 2 groups based on tumor diameter (cutoff, 30 post-vascular phase. Conclusion: We found that US imag-
mm). US imaging findings were retrospectively analyzed. ing features of HML differ depending on the tumor
Results: All tumors in patients with a small HML (<30 mm diameter. © 2017 S. Karger AG, Basel
in diameter, small group, n = 14) were revealed as homo-
129.127.145.224 - 12/11/2017 6:04:55 AM

© 2017 S. Karger AG, Basel Atsushi Hiraoka, MD, PhD


Gastroenterology Center
Ehime Prefectural Central Hospital
E-Mail [email protected]
83 Kasuga-cho, Matsuyama, Ehime 790-0024 (Japan)
www.karger.com/ddi
Univ.of Adelaide
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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
129.127.145.224 - 12/11/2017 6:04:55 AM

US Findings of HML Dig Dis 2017;35:498–505 499


DOI: 10.1159/000480138
Univ.of Adelaide
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Table 1. Clinical characteristics of tumor-forming hepatic malignant lymphoma divided by size

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

Dig Dis 2017;35:498–505


DOI: 10.1159/000480138
homogeneous
enhancement
4 67/M Secondary +/– 54 Hetero/hypo Unclear + + NE B-cell
lymphoma
(details
unknown)
5 84/F Secondary –/+ 52 Hetero/hypo Unclear + – NE DLBCL
6 40/M Secondary –/– 50 Hetero/hypo Clear + – NE DLBCL
7 36/M Primary –/– 33 Hetero/hypo Unclear – – Iso-vascular Iso-vascular Defect B-cell lymphoma
with avascular (details
area unknown)
8 53/M Secondary –/+ 33 Homo/hypo Clear – – Hypervascular Washout Defect DLBCL
homogeneous
enhancement
9 90/M Secondary –/– 32 Hetero/hypo Unclear + + Hypervascular Washout Defect DLBCL
spoke-wheel
pattern

 
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)

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

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-

Dig Dis 2017;35:498–505


DOI: 10.1159/000480138
enhancement
22 69/F Primary –/– 11 Homo/hypo Clear – – Hypervascular Washout Defect DLBCL + MALT
basket pattern
23 55/M Secondary –/– 10 Homo/hypo Clear – – Iso-vascular Washout Defect Adult T-cell
homogeneous- lymphoma
enhancement
24 64/M Secondary +/– 10 Homo/hypo Clear – – Iso-vascular Washout Defect DLBCL
homogeneous-
enhancement
25 74/M Secondary –/– 7 Homo/hypo Clear – – NE Hodgkin’s
lymphoma

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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129.127.145.224 - 12/11/2017 6:04:55 AM
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).

Representative Cases Case 2. A 73-year-old Japanese female was referred to


Case 1. An 89-year-old Japanese female was referred to Ehime Prefectural Central Hospital due to lymphadenopa-
Ehime Prefectural Central Hospital with elevated liver en- thy. A hepatic tumor (15 mm in diameter) was detected in
zymes. A hepatic tumor (32 mm in diameter) was detected the fifth segment of the liver by conventional US (Fig. 2),
in the second segment of the liver and revealed as a hetero- and lymphadenopathy was shown in full-body CT scan.
geneous hypo-echoic nodule with an unclear boundary The tumor was revealed as a homogeneous hypo-echoic
(Fig. 1). Intraperitoneal lymphadenopathy and pancreatic nodule with a clear boundary in conventional US images.
mass were shown in full-body CT scan. Penetrating sign was With CEUS, homogeneous enhancement in the early vas-
detected inside of the tumor and dilatation of the intrahe- cular phase and a washout pattern in the portal phase were
patic bile duct by tumor was also observed. Pathologically, observed, respectively. The tumor was revealed as a defect
the tumor was diagnosed as secondary hepatic DLBCL, in- in the post-vascular phase. The tumor was diagnosed as
cluding microscopic findings showing diffuse proliferation secondary hepatic DLBCL, with microscopic findings in-
of medium-to-large atypical lymphocytes with hematoxy- cluding diffuse proliferation of medium-to-large atypical
lin and eosin (H&E) staining, and positive findings for the lymphocytes with H&E staining, and positive findings for
anti-CD-20 antibody following immune staining. the anti-CD-20 antibody in immune staining.
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502 Dig Dis 2017;35:498–505 Kitahata  et al.


 

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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US Findings of HML Dig Dis 2017;35:498–505 503


DOI: 10.1159/000480138
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HML using US findings [20] and even with other modal- fection [24, 25], as they have been described as possible
ities [21, 22]. Lack of deterministic findings for US and trigger factors for immune activation, potentially leading
CEUS has been thought to be the reason why only a small to benign or malignant lymphoproliferative disorders.
number of patients have been reported with an HML. HBV or HCV infection was detected in 44% of the present
In general, an HML is revealed as a homogeneous hy- cohort. When a hepatic tumor is revealed as typical HCC
po-echoic lesion [1–3], and often includes the portal vein in CEUS findings but as a homogeneous hypo-echoic le-
or hepatic vein inside of the tumor without invasion (pen- sion in patients with chronic HBV or HCV infection,
etrating sign) in conventional US findings [4, 5]. Based on HML should be kept in mind for differential diagnosis. As
the present results, image findings of HML might differ confirmed by the present results, diagnosis of HML is of-
depending on the tumor diameter. In our study, small tu- ten difficult with only US and CEUS imaging, and remains
mors (<30 mm in diameter) were revealed as homoge- an important issue, indicating the importance of the role
neous hypo-echoic lesions, the same as previously report- of a pathological examination for obtaining a definitive
ed, whereas penetrating sign [5] was not detected in near- diagnosis. Of course, when a typical small-sized (<30 mm)
ly all cases. On the contrary, in large tumors (≥30 mm in HCC is shown to be clear homogenous hypo-echoic with
diameter) penetrating sign was detected, though 91% a clear boundary in conventional US, biopsy and general
(10/11) were revealed as a heterogeneous hypo-echoic le- examinations for screening of the lymph nodes including
sion. In addition, dilatation of the distal intrahepatic bile imaging should be considered [26, 27].
duct by tumor was observed in 4 cases, making it difficult To the best of our knowledge, no previous reports have
to distinguish it from CCC. noted differences in image findings of HML obtained
Trenker et al. [23] reported that HML had no specific with US and CEUS. It is important to keep in mind that
tendencies in CEUS findings for the early vascular and US findings vary according to tumor size in cases of pri-
post-vascular phases. In the present cohort, image findings mary and secondary HML. A limitation of the present
in the early vascular phase of CEUS for the large group var- study is the small number of patients. Thus, our findings
ied, while those for the small group nearly always showed are too limited for definitive conclusions. Therefore, ac-
an enhanced homogeneity and a washout pattern in the cumulation of cases and studies with a greater number of
portal phase, and defect in the post-vascular phase. Our patients is needed.
results also suggest that CEUS findings can differ accord-
ing to tumor size. In US and CEUS imaging, similar ten-
dencies were observed in both types of tumor-forming Disclosure Statement
HML according to tumor size (<30 or ≥30 mm; Table 2). There are no financial disclosures, grants from any organs, con-
Past reports have suggested that development of an flicts of interest, and/or acknowledgements for the authors to
HML might be associated with chronic HBV or HCV in- declare.

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