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Comparison of Contrast-Enhanced Ultrasound versus Contrast-Enhanced Magnetic Resonance Imaging for the Diagnosis of Focal Liver Lesions Using the Liver Imaging Reporting and Data System
COMPARISON OF CONTRAST-ENHANCED ULTRASOUND VERSUS CONTRASTENHANCED MAGNETIC RESONANCE IMAGING FOR THE DIAGNOSIS OF FOCAL
LIVER LESIONS USING THE LIVER IMAGING REPORTING AND DATA SYSTEM
TAGEDPJIA-YU WANG,* SHAO-YANG FENG,y AI-JIAO YI,z DI ZHU,x JIAN-WEI XU,{ JUN LI,║
XIN-WU CUI,* and CHRISTOPH F. DIETRICH#TAGEDEND
* Sino-German Tongji-Caritas Research Center of Ultrasound in Medicine, Department of Medical Ultrasound, Tongji Hospital,
Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; y Department of Ultrasound, Sixth
People’s Hospital of Zhengzhou, Zhengzhou, China; z Department of Ultrasound, First People’s Hospital of Yueyang, Yueyang,
China; x Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology,
Wuhan, China; { Department of Ultrasound, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China; ║ Department of
Ultrasound, First Affiliated Hospital of Shihezi University, Shihezi, China; and # Department of Internal Medicine, Hirslanden Clinic,
Bern, Switzerland
(Received 2 June 2019; revised 18 January 2020; in final from 22 January 2020)
Abstract—The aim of this retrospective study was to evaluate the Liver Imaging Reporting and Data System (LIRADS) categorization of focal liver lesions (FLLs) on contrast-enhanced ultrasound (CEUS) in comparison with
contrast-enhanced magnetic resonance imaging (CE-MRI). A total of 63 patients with 84 FLLs were included in
the final study population, after review of the electronic medical records and clinical data. Two trained radiologists evaluated all CEUS and CE-MRI images independently. They assigned a LI-RADS category to each FLL
and assessed major features based on CEUS LI-RADS phiên bản 2017 and computed tomography/MRI LI-RADS
Version 2018. The generalized estimating equation method was used to compare the diagnostic performance of
the LI-RADS algorithm between CEUS and CE-MRI. The sensitivity of LR-5/LR-TIV (tumor in vein) categories
for diagnosing hepatocellular carcinoma (HCC) differed significantly between CEUS and CE-MRI (88.9% [40/
45], 95% confidence interval [CI]: 76.5%95.2%), versus 64.4% (29/45; 95% CI: 49.8%76.8%), p = 0.006;
82.2% (37/45; 95% CI: 68.7%90.7%), versus 62.2% (28/45; 95% CI: 47.6%74.9%), p = 0.034. Inter-observer
agreement was substantial for assigning LR-5 on both CEUS and CE-MRI. For both reviewers, there was a
higher frequency of LR-5 (44.0% vs. 25.0%, p = 0.009; 42.9% vs. 26.2%, p = 0.023) in CEUS compared with CEMRI. Arterial phase hyper-enhancement (APHE) was less frequently observed on CEUS than on CE-MRI
(46.4% vs. 61.9%, p = 0.044). However, the washout appearance was observed more frequently on CEUS than on
CE-MRI (50.0% vs. 28.6%, p = 0.004). Inter-observer agreement between the two reviewers on APHE and washout appearance was excellent for both CEUS and CE-MRI. These findings suggest that CEUS had a much higher
sensitivity than CE-MRI in the diagnosis of HCC using LI-RADS, and although the frequencies of major features
differed, inter-observer agreement between the two reviewers on major features of HCC was excellent for both
CEUS and CE-MRI. (E-mail: [email protected]) © 2020 World Federation for Ultrasound in Medicine &
Biology. All rights reserved.
Key Words: Contrast-enhanced ultrasound, Magnetic resonance imaging, Liver Imaging Reporting and Data
System, Diagnosis, Liver.
INTRODUCTION
Liver cancer is the second leading cause of cancer mortality worldwide (Jemal et al. 2011; Torre et al. 2016; Forner
et al. 2018). Hepatocellular carcinoma (HCC) accounts for
70%90% of primary liver cancers globally and represents a major international health problem (Torre et al.
2016). HCC is most often caused by chronic infection
with hepatitis B virus (HBV) or hepatitis C virus (HCV)
(El-Serag 2011). In most cases, diagnosis of HCC can be
established by imaging examinations based on guidelines
promulgated by American Association for the Study of
Liver Diseases (Marrero et al. 2018) and the European
Address correspondence to: Xin-Wu Cui, Sino-German TongjiCaritas Research Center of Ultrasound in Medicine, Department of
Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1095 Jie Fang Avenue,
Wuhan 430030, China. E-mail: [email protected]
Association for the Study of the Liver (Galle et al. 2018).
The diagnostic imaging characteristics of HCC on contrast-enhanced ultrasound (CEUS), computed tomography
(CT) and magnetic resonance imaging (MRI) include arterial phase enhancement with portal venous phase or
delayed venous phase washout (Willatt et al. 2008; Lee
et al. 2015; Kee and Lu 2017).
To standardize the interpretation and reporting of
HCC, the American College of Radiology convened a
group of international experts to develop the Liver Imaging Reporting and Data System (LI-RADS) to reduce
variability in imaging reports and improve communication with clinicians. LI-RADS provides a comprehensive
algorithm including major features (lesion size, enhancement pattern, timing and degree of washout) and ancillary features that can be used to classify liver
observations by their likelihood of being HCC, ranging
from definitely benign (LI-RADS category 1 [LR-1]) to
definitely HCC (LR-5). If a solid nodule is definitely or
probably malignant but not HCC specific, it is assigned
as LR-M. LR-TIV represents definite tumor in the vein.
The LI-RADS was initially designed to be used with
the liver protocols of both CT and MRI in 2011. CEUS
LI-RADS was first published in 2016. Several amendments and updates have been made since then (Mitchell
et al. 2015; Tang et al. 2015). Although the CEUS LIRADS concept and principles for focal liver lesion (FLL)
characterization are similar to those for CT or MRI, there
are significant differences between CT/MRI LI-RADS and
CEUS LI-RADS. It is unclear whether the characterization
and reporting of FLLs using LI-RADS differ depending
on the imaging modality. For this reason, the choice of
imaging modality could affect subsequent clinical management. However, there are few related studies concerning these problems at present. Our study compares CEUS
LI-RADS with MRI LI-RADS to Giúp clinicians achieve
a deep understanding of LI-RADS and choose the appropriate imaging modality.
The aim of this retrospective study was to evaluate
LI-RADS categorization of FLLs on CEUS in comparison with that on contrast-enhanced magnetic resonance
imaging (CE-MRI).
METHODS
Patients
This retrospective study was approved by the local
institutional ethics review board, with waiver of patient
consent. A total of 63 patients with 84 FLLs evaluated
between July 2016 and October 2017 were included in
the final study population, after reviewing the electronic
medical records and clinical data. In our study, 45
patients had 1 nodule, 15 patients had 2 nodules and 3
patients had 3 nodules. And in those with multiple
nodules, the nodules were not close to each other. Inclusion criteria were as follows: (i) Patients had to be at
high risk for HCC according to LI-RADS (Kono et al.
2017; Chernyak et al. 2018); (ii) visible lesions had to
have been investigated by both ultrasound (US) and
MRI; and (iii) complete electronic patient records and
clinical data had to be available. Patients were excluded
on the basis of the following criteria: (i) systematic treatment for HCC before imaging examinations, which may
have influenced image interpretation; (ii) nodules too
tiny to be evaluated; and (iii) allergy to contrast agent
used in US or MRI.
Image acquisition: CEUS
All liver CEUS examinations included in this retrospective study were performed using the Hitachi Hi
Vision Avius (Hitachi Aloka Medical, Tokyo Japan). All
patients underwent conventional B-mode and Doppler
US before CEUS. CEUS examinations were performed
according to WFUMB (World Federation for Ultrasound
in Medicine and Biology) guidelines and good clinical
practice recommendations for CEUS of the liver (Claudon et al. 2013). FLLs were characterized with lowmechanical-index CEUS according to a standardized
protocol, that is, an intravenous bolus injection of
2.4 mL of SonoVue (Bracco, Milan Italy) followed by a
flush of 0.9% normal saline. Essential video clips were
recorded more than 46 min from the first arrival of
detected microbubbles to the later clearance. Vascular
phases were defined according to CEUS LI-RADS
(Kono et al. 2017).
Image acquisition: CE-MRI
All CE-MRI images included in this retrospective
study were acquired with 1.5-T MRI scanner systems
(Optima MR360, GE Healthcare) with phased-array
torso coils. All examinations included the following
unenhanced breath-holding axial-section sequences: T1-
weighted gradient echo in- and out-of-phase sequences
and T2-weighted fast spin-echo sequence. CE-MRI was
performed after intravenous injection of gadopentetate
dimeglumine (Magnevist, Bayer Schering Pharma AG,
Berlin, Germany) at a dose of 0.1 mmol/kg at the rate of
2 mL/s, followed by a 20-mL normal saline flush at the
same rate. Gadopentetate dimeglumine is the first choice
of contrast agent for hepatic CE-MRI in China. Because
of the retrospective nature of our study, we chose
patients who had all received MRI examinations using
gadopentetate dimeglumine to avoid the influence of a
different contrast agent. Two patients underwent gadoxetic acid-enhanced MRI were excluded from our study.
Hepatic arterial phase images were obtained automatically when the contrast agent reached the ascending
aorta. The portal venous phase images were obtained
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Comparison of Contrast-Enhanced Ultrasound versus Contrast-Enhanced Magnetic Resonance Imaging for the Diagnosis of Focal Liver Lesions Using the Liver Imaging Reporting and Data System
COMPARISON OF CONTRAST-ENHANCED ULTRASOUND VERSUS CONTRASTENHANCED MAGNETIC RESONANCE IMAGING FOR THE DIAGNOSIS OF FOCAL
LIVER LESIONS USING THE LIVER IMAGING REPORTING AND DATA SYSTEM
TAGEDPJIA-YU WANG,* SHAO-YANG FENG,y AI-JIAO YI,z DI ZHU,x JIAN-WEI XU,{ JUN LI,║
XIN-WU CUI,* and CHRISTOPH F. DIETRICH#TAGEDEND
* Sino-German Tongji-Caritas Research Center of Ultrasound in Medicine, Department of Medical Ultrasound, Tongji Hospital,
Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; y Department of Ultrasound, Sixth
People’s Hospital of Zhengzhou, Zhengzhou, China; z Department of Ultrasound, First People’s Hospital of Yueyang, Yueyang,
China; x Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology,
Wuhan, China; { Department of Ultrasound, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China; ║ Department of
Ultrasound, First Affiliated Hospital of Shihezi University, Shihezi, China; and # Department of Internal Medicine, Hirslanden Clinic,
Bern, Switzerland
(Received 2 June 2019; revised 18 January 2020; in final from 22 January 2020)
Abstract—The aim of this retrospective study was to evaluate the Liver Imaging Reporting and Data System (LIRADS) categorization of focal liver lesions (FLLs) on contrast-enhanced ultrasound (CEUS) in comparison with
contrast-enhanced magnetic resonance imaging (CE-MRI). A total of 63 patients with 84 FLLs were included in
the final study population, after review of the electronic medical records and clinical data. Two trained radiologists evaluated all CEUS and CE-MRI images independently. They assigned a LI-RADS category to each FLL
and assessed major features based on CEUS LI-RADS phiên bản 2017 and computed tomography/MRI LI-RADS
Version 2018. The generalized estimating equation method was used to compare the diagnostic performance of
the LI-RADS algorithm between CEUS and CE-MRI. The sensitivity of LR-5/LR-TIV (tumor in vein) categories
for diagnosing hepatocellular carcinoma (HCC) differed significantly between CEUS and CE-MRI (88.9% [40/
45], 95% confidence interval [CI]: 76.5%95.2%), versus 64.4% (29/45; 95% CI: 49.8%76.8%), p = 0.006;
82.2% (37/45; 95% CI: 68.7%90.7%), versus 62.2% (28/45; 95% CI: 47.6%74.9%), p = 0.034. Inter-observer
agreement was substantial for assigning LR-5 on both CEUS and CE-MRI. For both reviewers, there was a
higher frequency of LR-5 (44.0% vs. 25.0%, p = 0.009; 42.9% vs. 26.2%, p = 0.023) in CEUS compared with CEMRI. Arterial phase hyper-enhancement (APHE) was less frequently observed on CEUS than on CE-MRI
(46.4% vs. 61.9%, p = 0.044). However, the washout appearance was observed more frequently on CEUS than on
CE-MRI (50.0% vs. 28.6%, p = 0.004). Inter-observer agreement between the two reviewers on APHE and washout appearance was excellent for both CEUS and CE-MRI. These findings suggest that CEUS had a much higher
sensitivity than CE-MRI in the diagnosis of HCC using LI-RADS, and although the frequencies of major features
differed, inter-observer agreement between the two reviewers on major features of HCC was excellent for both
CEUS and CE-MRI. (E-mail: [email protected]) © 2020 World Federation for Ultrasound in Medicine &
Biology. All rights reserved.
Key Words: Contrast-enhanced ultrasound, Magnetic resonance imaging, Liver Imaging Reporting and Data
System, Diagnosis, Liver.
INTRODUCTION
Liver cancer is the second leading cause of cancer mortality worldwide (Jemal et al. 2011; Torre et al. 2016; Forner
et al. 2018). Hepatocellular carcinoma (HCC) accounts for
70%90% of primary liver cancers globally and represents a major international health problem (Torre et al.
2016). HCC is most often caused by chronic infection
with hepatitis B virus (HBV) or hepatitis C virus (HCV)
(El-Serag 2011). In most cases, diagnosis of HCC can be
established by imaging examinations based on guidelines
promulgated by American Association for the Study of
Liver Diseases (Marrero et al. 2018) and the European
Address correspondence to: Xin-Wu Cui, Sino-German TongjiCaritas Research Center of Ultrasound in Medicine, Department of
Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1095 Jie Fang Avenue,
Wuhan 430030, China. E-mail: [email protected]
Association for the Study of the Liver (Galle et al. 2018).
The diagnostic imaging characteristics of HCC on contrast-enhanced ultrasound (CEUS), computed tomography
(CT) and magnetic resonance imaging (MRI) include arterial phase enhancement with portal venous phase or
delayed venous phase washout (Willatt et al. 2008; Lee
et al. 2015; Kee and Lu 2017).
To standardize the interpretation and reporting of
HCC, the American College of Radiology convened a
group of international experts to develop the Liver Imaging Reporting and Data System (LI-RADS) to reduce
variability in imaging reports and improve communication with clinicians. LI-RADS provides a comprehensive
algorithm including major features (lesion size, enhancement pattern, timing and degree of washout) and ancillary features that can be used to classify liver
observations by their likelihood of being HCC, ranging
from definitely benign (LI-RADS category 1 [LR-1]) to
definitely HCC (LR-5). If a solid nodule is definitely or
probably malignant but not HCC specific, it is assigned
as LR-M. LR-TIV represents definite tumor in the vein.
The LI-RADS was initially designed to be used with
the liver protocols of both CT and MRI in 2011. CEUS
LI-RADS was first published in 2016. Several amendments and updates have been made since then (Mitchell
et al. 2015; Tang et al. 2015). Although the CEUS LIRADS concept and principles for focal liver lesion (FLL)
characterization are similar to those for CT or MRI, there
are significant differences between CT/MRI LI-RADS and
CEUS LI-RADS. It is unclear whether the characterization
and reporting of FLLs using LI-RADS differ depending
on the imaging modality. For this reason, the choice of
imaging modality could affect subsequent clinical management. However, there are few related studies concerning these problems at present. Our study compares CEUS
LI-RADS with MRI LI-RADS to Giúp clinicians achieve
a deep understanding of LI-RADS and choose the appropriate imaging modality.
The aim of this retrospective study was to evaluate
LI-RADS categorization of FLLs on CEUS in comparison with that on contrast-enhanced magnetic resonance
imaging (CE-MRI).
METHODS
Patients
This retrospective study was approved by the local
institutional ethics review board, with waiver of patient
consent. A total of 63 patients with 84 FLLs evaluated
between July 2016 and October 2017 were included in
the final study population, after reviewing the electronic
medical records and clinical data. In our study, 45
patients had 1 nodule, 15 patients had 2 nodules and 3
patients had 3 nodules. And in those with multiple
nodules, the nodules were not close to each other. Inclusion criteria were as follows: (i) Patients had to be at
high risk for HCC according to LI-RADS (Kono et al.
2017; Chernyak et al. 2018); (ii) visible lesions had to
have been investigated by both ultrasound (US) and
MRI; and (iii) complete electronic patient records and
clinical data had to be available. Patients were excluded
on the basis of the following criteria: (i) systematic treatment for HCC before imaging examinations, which may
have influenced image interpretation; (ii) nodules too
tiny to be evaluated; and (iii) allergy to contrast agent
used in US or MRI.
Image acquisition: CEUS
All liver CEUS examinations included in this retrospective study were performed using the Hitachi Hi
Vision Avius (Hitachi Aloka Medical, Tokyo Japan). All
patients underwent conventional B-mode and Doppler
US before CEUS. CEUS examinations were performed
according to WFUMB (World Federation for Ultrasound
in Medicine and Biology) guidelines and good clinical
practice recommendations for CEUS of the liver (Claudon et al. 2013). FLLs were characterized with lowmechanical-index CEUS according to a standardized
protocol, that is, an intravenous bolus injection of
2.4 mL of SonoVue (Bracco, Milan Italy) followed by a
flush of 0.9% normal saline. Essential video clips were
recorded more than 46 min from the first arrival of
detected microbubbles to the later clearance. Vascular
phases were defined according to CEUS LI-RADS
(Kono et al. 2017).
Image acquisition: CE-MRI
All CE-MRI images included in this retrospective
study were acquired with 1.5-T MRI scanner systems
(Optima MR360, GE Healthcare) with phased-array
torso coils. All examinations included the following
unenhanced breath-holding axial-section sequences: T1-
weighted gradient echo in- and out-of-phase sequences
and T2-weighted fast spin-echo sequence. CE-MRI was
performed after intravenous injection of gadopentetate
dimeglumine (Magnevist, Bayer Schering Pharma AG,
Berlin, Germany) at a dose of 0.1 mmol/kg at the rate of
2 mL/s, followed by a 20-mL normal saline flush at the
same rate. Gadopentetate dimeglumine is the first choice
of contrast agent for hepatic CE-MRI in China. Because
of the retrospective nature of our study, we chose
patients who had all received MRI examinations using
gadopentetate dimeglumine to avoid the influence of a
different contrast agent. Two patients underwent gadoxetic acid-enhanced MRI were excluded from our study.
Hepatic arterial phase images were obtained automatically when the contrast agent reached the ascending
aorta. The portal venous phase images were obtained
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