Hepatobiliary Pancreatic Diseases International

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JID: HBPD [m5G; November 6, 2018;13:49 ]

Hepatobiliary & Pancreatic Diseases International xxx (xxxx) xxx

Contents lists available at ScienceDirect

Hepatobiliary & Pancreatic Diseases International

journal homepage: www.elsevier.com/locate/hbpd

Original Article/Liver

Potential application of ultrasound-guided thermal ablation in rare

liver tumors

Li-Li Wu

a , Jia-Xin Chen

a , Kai Li a , Zhong-Zhen Su

b , Ying-Lin Long

a , Li-Ping Luo

a , Er-Jiao Xu

a , ∗, Rong-Qin Zheng

a

a Department of Medical Ultrasonics, Third Affiliated Hospital of Sun Yat-sen University, Guangdong Key Laboratory of Liver Disease Research, Guangzhou

510630, China b Department of Medical Ultrasonics, Fifth Affiliated Hospital of Sun Yat-sen University, Zhuhai 5190 0 0, China

a r t i c l e i n f o

Article history:

Received 4 May 2018

Accepted 15 October 2018

Available online xxx

Keywords:

Contrast-enhanced ultrasound

Thermal ablation

Rare liver tumor

Fusion imaging

a b s t r a c t

Background: With the advances of imaging techniques, the detection rate of rare liver tumor is increased.

However, the therapeutic strategies of the rare liver tumors remain limited.

Methods: We analyzed twelve pathologically confirmed rare liver tumors in 8 patients. All of the pa-

tients underwent ultrasound (US) guided biopsy and subsequent thermal ablation. The tumors were ab-

lated according to the preoperative plans and monitored by real-time US. CT/MRI fused with contrast

enhanced US (CEUS) or three-dimensional (3D) US-CEUS images were used to guide and assess the abla-

tion zone more accurately during thermal ablation. The rate of technical efficacy was assessed based on

the contrast-enhance CT/MRI (CECT/MRI) results one month after ablation. Local tumor progression (LTP),

recurrence and complications were followed up and recorded.

Results: Among these twelve nodules, nine were subject to US-guided thermal ablation, whereas

the other three inconspicuous nodules were subject to CEUS-guided thermal ablation. Intra-procedure

CT/MRI-CEUS or 3D US-CEUS fusion imaging assessments demonstrated that the ablation zone sufficiently

covered the original tumor, and no immediate supplementary ablation was required. Additionally, no ma-

jor complications were observed during the follow-up period. The postoperative CECT/MRI confirmed that

the technique success rate was 100%. Within the surveillance period of 13 months, no LTP or recurrence

was noted.

Conclusions: US-guided thermal ablation was feasible and safe for rare liver tumors. The use of fusion

imaging technique might make US-guided thermal ablation as effective as surgical resection, and this

technique might serve as a potential therapeutic modality for rare liver tumors in the future.

© 2018 First Affiliated Hospital, Zhejiang University School of Medicine in China. Published by Elsevier

B.V. All rights reserved.

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1

ntroduction

Liver cancer is the second leading cause of death from cancer

orldwide, and the diagnosis and treatment of this cancer are crit-

cal [1–3] . The International Classification of Diseases by the WHO

ites various types of liver tumors. The most common types in-

lude hepatocellular carcinoma (HCC), intrahepatic cholangiocarci-

oma (ICC), liver metastasis from colorectal cancer and hepatic he-

angioma [4] . In addition, there are a number of rare liver tumors

ith a low incidence. These types of liver tumors are histologically

iverse and clinically asymptomatic, and their diagnoses rely con-

iderably on histological examination. However, some of these liver

umors are malignant or borderline, and removal of these liver

∗ Corresponding author.

E-mail address: [email protected] (E.-J. Xu).

n

t

ttps://doi.org/10.1016/j.hbpd.2018.10.002

499-3872/© 2018 First Affiliated Hospital, Zhejiang University School of Medicine in Chin

Please cite this article as: L.-L. Wu, J.-X. Chen and K. Li et al., Potentia

tumors, Hepatobiliary & Pancreatic Diseases International, https://doi.o

umors is necessary. Due to the low incidence of rare liver tu-

ors and the lack of symptoms or biochemical indices, it is dif-

cult to differentiate these tumors in preoperative imaging exami-

ation. Hence, the golden standard for the diagnosis is histology.

Prior studies have demonstrated that ultrasound (US) guided

hermal ablation is as effective as resection for early-stage HCC

ith respect to the long-term survival rate [5 , 6] . Additionally, ther-

al ablation is superior given its increased safety, reduced compli-

ations and more rapid recovery. The 2014 Japanese guidelines for

he treatment of liver cancer recommended radiofrequency abla-

ion as a first-line treatment for early HCC [7] . Nevertheless, the

pplication of thermal ablation in rare liver tumors has not been

ssessed to date.

In the present study, we retrospectively analyzed the effective-

ess of US-guided thermal ablation on the treatment of rare liver

umors.

a. Published by Elsevier B.V. All rights reserved.

l application of ultrasound-guided thermal ablation in rare liver

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2 L.-L. Wu, J.-X. Chen and K. Li et al. / Hepatobiliary & Pancreatic Diseases International xxx (xxxx) xxx

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Table 1

Demographic and examination data of the rare liver tumor cases.

Case no. Age (yr) Gender Lesion no. Position Diameter (mm) Pathology Ablation technique

1 29 F 1 S5 25 Inflammatory pseudotumor-like follicular dendritic cell RFA

2 47 F 2 S8 14 Inflammatory myofibroblastic tumor RFA

3 46 F 3 S4 22 Inflammatory myofibroblastic tumor RFA

4 64 F 4 S5 21 Mucosa-associated lymphoid tissue lymphomas RFA

5 S2 9

6 S4 7

5 34 F 7 S4 8 Metastasis of spleen inflammatory myofibroblastic tumor RFA

8 S7/8 13

6 28 M 9 S6/7 14 Tissue cells and dendritic cell tumors RFA

7 49 F 10 S5/8 14 B-cell-derived lymphoma or dendritic cell tumor RFA

11 S2 6

8 47 M 12 S8 22 EBV-associated lymphoepithelioma-like cholangiocarcinoma MWA

F: female; M: male; RFA: radiofrequency ablation; MWA: microwave ablation.

Table 2

Conventional US characteristics and contrast-enhanced US patterns of liver nodule.

Case

No.

Lesion

No.

Echogenicity Margin CEUS pattern

Arterial

phase

Portal

phase

Delay

phase

1 1 Hypo-echoic Clear Hyper- Hypo- Hypo-


3 3 Hypo-echoic Obscure Hyper- Iso- Iso-


5 Hypo-echoic Clear Iso- Hypo- Hypo-

6 Iso-echoic Obscure Hyper- Hypo- Hypo-


8 Hypo-echoic Clear Hyper- Hypo- Hypo-

6 9 Hypo-echoic Obscure Hyper- Hypo- Hypo-


11 Hypo-echoic Clear Hyper- Hypo- Hypo-


US: ultrasound; CEUS: contrast-enhanced ultrasound.

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Methods

Patients

This study was performed in compliance with the Declaration

of Helsinki and approved by the Institutional Ethics Review Board

of the Third Affiliated Hospital of Sun Yat-sen University. Informed

consent of ablation was obtained from each patient. Informed con-

sent of this study was waived due to the retrospective nature of

the study. All procedures were performed by two proficient radi-

ologists (LK and XEJ) with more than 10 years of experience in US

and US-guided thermal ablation.

Recruited patients included those who were diagnosed with

rare liver tumors by pathological examination and subsequently re-

ceived US-guided thermal ablation in our hospital from January

2014 to December 2016. The inclusion criteria were as follows:

(1) histological confirmation of rare liver tumors; (2) a single tu-

mor with a diameter ≤ 5 cm or less than 3 tumor nodules with the

maximal diameter ≤ 3 cm; (3) no invasion to major vessels or bile

ducts, adjacent or distant tissues/organs; (4) Child-Pugh Class A or

B liver function; and (5) underwent US-guided liver thermal ab-

lation successfully. The exclusion criteria were as follows: (1) de-

ficiency of the pre-procedure or intra-procedure imaging data re-

sulting in unanalyzable; and (2) without contrast-enhance CT/MRI

(CECT/CEMRI) evaluation one month after ablation and regular

follow-up every three months.

All the included lesions were confirmed by histology that were

obtained by US-guided tumor biopsy shortly before liver thermal

ablation. U



ltrasound-guided thermal ablation

quipment

Two types of thermal ablation were performed in this study:

adiofrequency ablation (RFA) and microwave ablation (MWA).

he former employed a Radionics Cool-tip RFA System (Valley-

ab, Mansfield, MA, USA) with a maximal output power of 200 W

nd single-pole, internally cooled ablation needles with 3-cm tips.

he latter employed a KY-20 0 0 Water-cooled MWA Instrument

Kangyou Co., Nanjing, China) comprising a microwave generator

ith an emission frequency of 2450 ± 50 MHz, output power of

0–100 W, and a 15-G water-cycle internally cooled microwave an-

enna.

Two types of US apparatuses with CnTI contrast-specific imag-

ng, namely, MyLab Twice and MyLab ClassC (Esoate, Genoa, Italy),

ere employed. Convex probes CA431 and CA541 (frequency: 1–

MHz) were used for US scanning and guidance. The fusion imag-

ng system Virtual Navigator (VN; Esoate) was composed of a main

nit in the US machine, a corresponding probe sensor adhered to

he probe and a magnetic field generator. The dedicated software

as installed on the US machine. The magnetic field generator and

he probe sensor ensured the exact position between the sensor

nd the patient.

ontrast-enhanced US (CEUS)

SonoVue (Bracco, Milan, Italy) was used for CEUS examination.

bolus of SonoVue (1.5–2.0 mL) was injected via the antecubital

ein, followed by 5 mL saline solution. When necessary, SonoVue

as injected repeatedly.

blation strategy

All patients were intubated with general anesthesia. After per-

utaneous biopsy, US-guided thermal ablation was conducted fol-

owing the preoperative plan. For RFA, the RF generator was set

o the impedance mode with maximal output, and each RF elec-

rode was inserted into the lesion within approximately 12 min. For

WA, the microwave generator was set to 60 W and maintained

or up to 6 min in each microwave antenna insertion.

Ablation was guided by real-time US or CEUS. When neces-

ary, ancillary means, such as the application of artificial ascites

nd artificial pleural fluids, were administered to improve le-

ion visualization and prevent damage to the surrounding criti-

al organs and tissues. In our hospital, CT/MRI-US fusion imag-

ng, which combined CT or MRI images with real-time US im-

ges using the electromagnetic positioning system of VN, was

outinely employed for thermal ablation procedures. This method

ided in the detection of inconspicuous lesions, puncture guidance

nd immediate evaluation of therapeutic response. The CT/MRI-

S fusion imaging procedure included the outline of the index


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L.-L. Wu, J.-X. Chen and K. Li et al. / Hepatobiliary & Pancreatic Diseases International xxx (xxxx) xxx 3

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Fig. 1. A 47-year-old female patient with inflammatory myofibroblastic tumor. A –C : The contrast enhanced ultrasound (CEUS) images demonstrating the hyper-enhancement

in arterial phase and hypo-enhancement in portal phase; D –F : Preoperative MRI images demonstrating the hyper-enhancement in arterial phase and hypo-enhancement in

portal and venous phase; G : The 3D US-CEUS fusion imaging evaluation carried out immediately after the radiofrequency ablation showing the non-enhanced zone of CEUS

covered the blue ring of index tumor and the red ring of preset ablative margin, which indicated the tumor and its 5 mm ablative margin were completely ablated except

the adjacent large vessels; H : One month post-operatively, contrast enhanced MRI image showing the completely necrosis of the index tumor.

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esion and its ablative margins on CT/MRI images, registration of

wo sets of images, alignment by fine-tuning and navigation. The

etails of the procedure were described in our previous report [8] .

f the index lesion was inconspicuous, CT/MRI-US fusion imaging

ould be used to locate the lesion and guide the subsequent punc-

ure. After the thermal ablation procedure, CT/MRI-CEUS fusion

maging was generally employed to assess whether the ablated

one covered the index lesion and its ablative margin. If possi-

le, 5 mm ablative margin was required during intraoperative as-

essment unless the lesion was adjacent to the major hepatic ves-

els or liver capsule. Moreover, 3D US-CEUS fusion imaging was

lso used for the immediate evaluation of therapeutic response in

ome other patients if the lesions were conspicuous on US im-

ges. Briefly, 3D US-US fusion imaging fused the real-time US im-

ges with the 3D US images that were acquired before ablation
a


nd during the procedure using the VN electromagnetic position-

ng system. Details of the 3D US-CEUS fusion imaging procedure

ere also described in our previous report [9] .

ostoperative evaluation and follow-up

All patients underwent conventional US examination within

4–72 h after thermal ablation to exclude early-stage complica-

ions. CECT/CEMRI was performed one month after ablation to

ssess technique efficacy. A tumor was regarded to have been

ffectively ablated when there was no longer any enhancement

ithin the ablation zone during the arterial phase on CECT/CEMRI.

f any residual tumor was present, the residual tumor was

hen ablated and re-evaluated. If the ablation was considered to

chieve technique efficacy, the patient was followed up every


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Fig. 2. A 49-year-old female patient with B-cell-derived lymphoma or dendritic cell tumor. A–C: The preoperative MRI images demonstrating the hyper-enhancement in arte-

rial phase and hypo-enhancement in the portal and venous phase of the lesion; D –F : The contrast enhanced ultrasound (CEUS) images demonstrating the hyper-enhancement

in arterial phase and hypo-enhancement in the portal phase; G : The 3D US-CEUS fusion imaging evaluation carried out immediately after the radiofrequency ablation show-

ing the non-enhanced zone of CEUS covered the index tumor and the yellow ring of preset ablative margin, which indicated the tumor and its 5-mm ablative margin were

completely ablated; H : One month post-operatively, contrast enhanced MRI image showing the completely necrosis of the index tumor.

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three months after thermal ablation to evaluate recurrence and

complications.

Local tumor progression (LTP) was defined as the appearance of

new tumor foci one month after intervention at the edge of the ab-

lation zone, which was often characterized as hyper-enhancement

during arterial phase with hypo-enhancement in the portal venous

system or the delayed phase on CECT/CEMRI images.

Statistical analysis

All statistical analyses were performed using SPSS software

(Version 22.0, SPSS Inc., Chicago, IL, USA). Quantitative and qualita-

tive data were presented as the median (range) and number (per-

centage), respectively.



esults

emographic data of patients and lesions

In total, eight patients with twelve tumors were enrolled in this

tudy, including two male and six female patients with a median

ge of 47 (28–64) years. Among these eight patients, one had three

odules, and two patients had two nodules. Only one patient had a

istory of hepatitis B. The demographic and baseline data are pre-

ented in Table 1 . All of the nodules were confirmed by pathology

xamination.

In total, 91.7% (11/12) of the lesions presented as hypoechoic le-

ions on US images. In CEUS examinations, all of the lesions exhib-

ted “wash-out” features. In addition, 91.7% (11/12) of the lesions


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Fig. 3. A 46-year-old female patient with recurrent inflammatory myofibroblastic tumor. A –C : Preoperative MRI image of the index tumor; D : MRI-US fusion imaging located

the index tumor which was inconspicuous on US images before radiofrequency ablation; E : After the radiofrequency ablation, MRI-CEUS fusion imaging was employed to

evaluate the therapeutic effect immediately. The CEUS images showing the non-enhanced zone already covered the blue ring of index tumor and the red ring of preset

ablative margin, which indicated the tumor and 5-mm ablative margin were completely ablated; F : One month post-operatively, contrast enhanced MRI image showing the

completely necrosis of the index tumor.

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xhibited hyper-enhancement during the arterial phase and hypo-

nhancement during the portal phase or late phase.

S guidance and intra-procedure assessment of thermal ablation of

are liver tumors

rocedure of liver tumor thermal ablation

All the tumors included in this study were ablated precisely

t the designated regions. Among these twelve nodules, nine

ere subject to US-guided thermal ablation, whereas three incon-

picuous nodules were subject to CEUS-guided thermal ablation

Table 2 ). Artificial ascites was administered in one case to improve

esion visualization and prevent damages to the adjacent gastroin-

estinal tract.

According to the immediate evaluation of fusion imaging, the

on-perfusion zones covered the target lesions. Besides, at least 5-

m ablative margins were achieved unless the lesion was adjacent

o the major hepatic vessels or liver capsule. All the lesions were



onsidered to be completely ablated after a single ablation session.

he technical success rate was 100%. No early major complications

ccurred during the follow-up period of 72 h.

ollow-up and prognosis

One month later, CECT/CEMRI conducted on all patients con-

rmed complete necrosis in all lesions without major complica-

ions. The technique efficacy was 100% (12/12). The median follow-

p duration was 13 (2–32) months, and no LTP was observed

uring the follow-up period ( Figs. 1 and 2 ). Of note, one pa-

ient with an inflammatory myofibroblastic tumor underwent a

ight hepatectomy, and another lesion in left liver was detected

nd ablated in another hospital. However, 5 months later, tumor

ecurrence was noted in the left liver. In our hospital, RFA was

epeated, and the ablative margin was achieved upon evaluation

f MRI-CEUS fusion imaging ( Fig. 3 ). No additional recurrence oc-

urred during the follow-up period.


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Discussion

CECT or CEMRI is recognized as major imaging modality for the

differentiation of liver tumors [10] . However, for rare liver tumors,

the enhancement pattern was atypical, and only a few studies have

been reported. CEUS is a novel imaging modality that is an ef-

fective method for the differentiation of most common liver tu-

mors according to enhancement patterns [11–14] . However, only

a few reports have provided enhancement patterns of rare liver

tumors [15] . In our study, all the lesions were “wash-out” in the

portal/delay phase, indicating the malignant nature of the tumor

according to the CEUS-LI-RADS [16] . Therefore, the acquisition of

pathological confirmation and removal of the liver tumor were se-

lected as the treatment strategy. In this study, all the enrolled pa-

tients refused liver resection, and US-guided biopsy and thermal

ablation were recommended for these patients after multidisci-

plinary consultation.

Previous studies reported that the most common treatment for

rare liver tumors is surgery [17] . Traditional surgical intervention

suggests that not only the target tumor but also the surrounding

liver parenchyma should be resected to reduce tumor volume and

the risk of recurrence. However, the clinical application of liver

resection was largely limited due to serious surgical trauma and

long recovery time. Local thermal ablation achieves the therapeutic

effect by killing tumor cells using high temperature. Compared

with the traditional surgical treatment, percutaneous thermal ab-

lation of liver tumors can effectively reduce trauma and surgery-

related complications [18,19] . However, due to the limited ab-

lative region, residual or LTP was more common. Our previous

reports demonstrated that the fusion imaging technique was a use-

ful tool to improve the local curative effect of HCC. With the help

of CT/MRI-US fusion imaging or 3D US-US fusion imaging, the ab-

lative margin could be simultaneously outlined and displayed on

real-time US images [8,20] . After ablation, immediate evaluation

using CT/MRI-CEUS fusion imaging or 3D US-CEUS fusion imag-

ing could be employed to assess whether the ablative region cov-

ers the entire lesion and its surrounding ablative margin. Thus,

we could enlarge the ablative region as far as possible in a man-

ner similar to surgical resection to reduce residual and LTP. In this

study, no residual or LTP was noted in all the enrolled patients.

However, one patient with a splenic inflammatory myofibroblastic

tumor and liver metastases experienced recurrence after RFA treat-

ment, which was performed at another hospital. She underwent

RFA in our hospital such that the ablation region covered the target

tumor and the ablative margin under the guidance of CT/MRI-CEUS

fusion imaging. No recurrence was noted during the subsequent

15-month follow-up. Therefore, local thermal ablation is also feasi-

ble for rare liver tumors, and the fusion imaging technique might

allow US-guided thermal ablation to become as effective as surgi-

cal resection. The risk of trauma and complication could be also

greatly reduced with thermal ablation when compared with resec-

tion.

Nevertheless, some limitations of this study should be noted.

First, the number of cases involved is small partly due to the low

incidence of rare liver tumors. This limitation may lead to a bi-

ased conclusion. Second, the follow-up duration is relatively short.

Hence, the recurrence and survival rates could differ after a longer

period of observation despite the fact that all the cases experi-

enced successful and complete ablation of their tumors with no

recurrence during the specified follow-up period.

In conclusion, US-guided thermal ablation is feasible and safe

for rare liver tumors. The use of a fusion imaging technique might

allow US-guided thermal ablation to become as effective as sur-

gical resection and serve as a potential therapeutic mode for rare

liver tumors in the future.



ontributors

WLL, CJX and XEJ conceived, designed and performed the exper-

ments, analyzed the data, wrote the paper, and reviewed drafts of

he paper. LK, SZZ and ZRQ reviewed drafts of the paper. LYL and

LP collected the data. All the authors have read and approved this

ubmission. WLL and CJX contributed equally to this work. XEJ is

he guarantor.

unding

This study was supported by grants from National Key R&D Pro-

ram of China ( 2017YFC01120 0 0 ), National Natural Science Foun-

ation of China ( 81430038 and 81401434 ), Science and Technol-

gy Planning Project of Guangdong Province ( 2015A020214009 ,

016A020215072 , and 2017A020215082 ); and Natural Science

oundation of Guangdong Province ( 2016A030313205 ).

thical approval

This study was approved by the Institutional Ethics Review

oard of the Third Affiliated Hospital of Sun Yat-sen University.

ompeting interest

No benefits in any form have been received or will be received

rom a commercial party related directly or indirectly to the sub-

ect of this article.

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