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ORIGINAL ARTICLE

Transient Segmental Enhancement of Pyogenic Liver Abscess:


A Comparison Between Contrast-Enhanced Ultrasound
and Computed Tomography
Kun Sun, MD,* Wei Zhu, MD,† Yan Luo, MS,‡ Yongzhong Li, MD,‡ and Xiang Zhou, MD§

variable.1,2 However, a delayed diagnosis of hepatic abscess may


Objective: This study aimed to investigate the correlation between the lead to higher mortality rates. The patient with hepatic abscess
transient segmental enhancement (TSE) of liver abscesses on contrast- usually has high fever. Therefore, the diagnostic accuracy is high
enhanced ultrasound (CEUS) imaging and contrast-enhanced computed to- if the clinical features are combined with blood testing. However,
mography (CT) scans. some cases of hepatic malignant tumors, especially those that have
Methods: In total, 42 abscesses in 38 patients were evaluated with real- large areas of necrosis, also may have fever and be misdiagnosed
time CEUS and contrast-enhanced CT imaging. The CT imaging and as abscess. Therefore, it is important to use contrast-enhanced ul-
CEUS examinations were performed within one to 2 days of each other trasound (CEUS) for early diagnosis and initiate prompt therapy
in all cases. The initial reports of the observations of TSE on CEUS scans to reduce morbidity and mortality.
were correlated later with the findings of TSE on contrast-enhanced CT im- The diagnosis of hepatic abscesses has been improved by
ages. Contrast-enhanced CT was used as the reference standard to evaluate the use of ultrasonography and computed tomography (CT)
the presence of TSE. Relationships between the 2 groups were analyzed scans.2–4 Hepatic abscesses occasionally mimic the appear-
using the χ2 test. P < 0.05 was considered to be statistically significant. ances of other hepatic lesions such as metastases, in plain and
Results: In 16 patients, 16 typical TSE signs were shown by CEUS. contrast-enhanced CT and ultrasound (US) images. It is important
Meanwhile, enhanced CT imaging showed 18 typical signs of TSE in to differentiate abscesses from other lesions in order to initiate ap-
17 patients. We identified 38 patients with hepatic abscesses proven by propriate therapy. Several identifying features of hepatic abscesses
needle aspiration (10 patients) or image-guided biopsy (28 patients). Ten have been identified on CEUS and CT scans.2–9
patients had hepatobiliary cholelithiasis, 5 had diabetes mellitus type 2, Mathieu et al8 and Gabata et al10 reported that a transient seg-
and 2 had gastric cancer, whereas no evidence of underlying hepatobiliary mental wedge-shaped hepatic enhancement (TSE), which is asso-
or gastrointestinal diseases was found in the other 21 patients. Considering ciated with hepatic abscesses, is sometimes visible in the early
that enhanced CT is the reference standard for the diagnosis of hepatic phase of dynamic CT scanning and is of diagnostic value. The
abscesses, the sensitivity of CEUS in showing TSE was 89%, and the purpose of this study was to investigate the correlation between
specificity was 100%. The χ2 test indicated that CEUS and enhanced the presence of TSE due to liver abscesses on CEUS and
CT were significantly correlated for detection of hepatic perfusion contrast-enhanced CT scans. Therefore, we retrospectively ana-
disorders (P < 0.05). lyzed the CEUS and CT findings of TSE due to hepatic abscesses
Conclusions: The appearance of TSE in liver abscess was reliably in a cohort of patients from a single center.
detected by CEUS, which correlated well with the enhanced CT The purpose of this study was to determine the sensitivity of
images (P < 0.05). CEUS in detecting TSE by comparing the findings of helical CT
Key Words: contrast-enhanced ultrasound image, liver, with the findings of CEUS and to conduct a pathologic analysis of
transient segmental enhancement resected specimens.
(J Comput Assist Tomogr 2017;00: 00–00)
MATERIALS AND METHODS
P yogenic liver abscesses, caused by bacteria, result in localized
collection of pus and destruction of the surrounding hepatic
parenchyma.1 The epidemiology of pyogenic abscesses has
Patient Population
The study was approved by the research ethics board of West
changed significantly in the modern era of antibiotic usage. The
China Hospital, Sichuan University, China. Informed consent was
clinical manifestations of pyogenic hepatic abscesses are highly
obtained from all patients prior to enrollment in the study. Patients
with liver mass, fever, and inflammation as determined by periph-
From the *Department of Ultrasound, Shenzhen Hospital, Southern Medical
eral hemogram were selected for this study between April 2010
University, Guangdong; †Echo Lab of Cardiology Department/Department of and July 2014. Patients who had undergone liver CEUS examina-
Ultrasound, West China Hospital, Sichuan University; and ‡Department of Ultra- tion and contrast-enhanced CT within 1 to 2 days before or after
sound, West China Hospital, Chengdu, Sichuan; and §Department of Ultra- the CEUS examination were included in the study. The patients
sound, National Cancer Center/Cancer Hospital, Chinese Academy of
Medical Sciences and Peking Union Medical College, Beijing, China.
with more than 1 type of lesion, cardiac insufficiency, severe renal
Received for publication April 10, 2017; accepted June 5, 2017. dysfunction, hepatectomy, or splenectomy were excluded from the
Correspondence to: Xiang Zhou, MD, Department of Ultrasound, National study. The reasons for exclusion were patients with more than 1
Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and type of lesion in the liver because the blood supply in some tumors
Peking Union Medical College, No. 17 Panjiayuan Nanli, Chaoyang
District, Beijing 100021, China (e‐mail: zhou.xiang@yeah.net).
with abundant blood supply, such as hepatic hemangioma in addi-
K.S. and W.Z. contributed equally as joint first authors. tion to hepatocellular carcinoma, may affect the characteristics of
The authors declare no conflict of interest. CEUS. We excluded patients with severe renal or cardiac dysfunc-
This work was supported by the National Natural Science Foundation of China tion because of possible worsening of organ dysfunction by contrast
(NSFC grant 31170957) and the Sichuan Youth Science and Technology
Foundation (SYSTF grant 2012JQ0015).
agent. We excluded patients with severe renal dysfunction because
Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved. of possible worsening of organ perfusion because of severe water
DOI: 10.1097/RCT.0000000000000659 and sodium retention. Patients with cardiac insufficiency were

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Sun et al J Comput Assist Tomogr • Volume 00, Number 00, Month 2017

excluded because cardiac insufficiency may influence microcircu- accuracy analysis of CEUS, grades 1 and 2 were defined as nega-
lation perfusion. In this study, 1 patient with severe renal failure tive results, and grades 3, 4, and 5 were defined as positive results.
and 2 patients with heart failure were excluded from the study. Pa-
tients who did not undergo both examinations and who were treated CEUS Examinations
with antibiotics for more than 3 days were also excluded from the
study. All patients were prospectively selected on the basis of detec- All the ultrasonography studies were performed using a con-
tion of 1 or more hepatic abscesses, demonstrated by either CEUS vex probe (4 V1 vector transducer, 3–4 MHz; ACUSON Sequoia
or CT. 512; Siemens, Mountain View, Calif) equipped with cadence con-
We identified 38 patients with hepatic abscesses proven by trast pulse sequencing (CPS) technology software. After activation
needle aspiration (10 patients) or imaged-guided biopsy (28 pa- of the CPS-Mix mode with a low mechanical index (0.1–0.2) and ad-
tients). Ten patients had hepatobiliary cholelithiasis, 5 had diabe- aptation of image quality, a bolus injection of 2.4 mL of microbubble
tes mellitus type 2, and 2 patients had gastric cancer, whereas no SonoVue (Bracco Imaging BV, Geneva, Switzerland) was adminis-
evidence of underlying hepatobiliary or gastrointestinal diseases tered intravenously, followed by 5 mL of 0.9% saline solution.7 A
was found in the other 21 patients. There were 25 men and 13 3-way stopcock was used so that the saline flush could be admin-
women (male-to-female ratio 1.9:1.0) of median age 47 years istered immediately after the injection of contrast agent.
(range, 40–67 years).
CT Examinations
Imaging Analysis Dynamic CT scans were performed using a 64-channel
Computed tomography imaging and CEUS examination multi–detector-row CT scanner (Brilliance 64-channel CT;
were performed within 1 to 2 days of each other in all cases. Philips Medical Systems, Cleveland, Ohio) and two 16-channel
The CT and CEUS examinations were performed 1 or 2 days be- CT scanners (Brilliance 16-channel CT [Philips Medical Systems]
fore the diagnosis of liver abscess, so the likelihood of a change in and Siemens Sensation 16 [Siemens Co, Erlangen, Germany]).
the abscess before the clinical treatment was obtained was low. All Unenhanced and contrast-enhanced dynamic CT scans were ob-
CEUS was performed by 1 diagnostic radiologist (X.Z.) who had tained. kVp of the x-ray tube was 100 to 120. Dynamic CT imag-
10 years of experience in US diagnosis and with knowledge of the ing was initiated 30 seconds (early phase) and 90 seconds (late
histological diagnosis of abscess by a biopsy or pus extraction phase) after the injection of Omnipaque 350 (GE Healthcare,
with hematoxylin-eosin staining or cytology and CT findings. Nycomed Amersham, Princeton, NJ) contrast medium was initi-
There were necrosis of liver tissue and pus in abscess cavities by ated. Subsequently, 100 mL of contrast medium was injected at
cytology report. Biopsy from abscesses showed abscess walls a rate of 3 mL/s with a power injector.11
formed by fibrous granulation tissue and hyperplasia by patho-
logic report. The examinations were interpreted by consensus of Statistical Analysis
2 radiologists (W.Z. and Y. Li) who were blinded to the CT and The statistical study was based on a single-lesion-per-patient
histology results. The initial reports of the observations of TSE analysis. Statistical analyses were performed by using software
on CEUS scans were correlated later with the findings of TSE (SPSS version 10.1; SPSS, Chicago, Ill). For all tests, (P < 0.05)
on contrast-enhanced CT scans. Contrast-enhanced CT was used was considered to indicate a statistically significant difference.
as the reference standard for evaluation of the presence of TSE Weighted κ statistics were used to evaluate the hypothesis of con-
and to validate the findings on CEUS images. sistency between contrast-enhanced CT and CEUS. Agreement
was graded as poor (κ < 0.20), fair (κ = 0.20 to <0.40), moderate
Evaluation of Interreader Agreement (κ = 0.40 to <0.60), good (κ = 0.60 to <0.8), and very good
Digital CEUS cine clips or images stored on digital disks (κ = 0.80–1). The sensitivity, specificity, positive and negative pre-
were reviewed separately by 2 independent radiologists (W.Z. dictive values, and accuracy for detection of TSE were calculated
and K.S., with 4 years of experience in CEUS, respectively) using based on the consensus of 2 CEUS readers.
viewing software (Showcase [Trillium Technology, Ann Arbor,
Mich] and QLAB [Philips Healthcare, Bothell, Wash]). For each RESULTS
lesion, 2 readers were asked to give a diagnostic score of TSE after Of 38 patients, 36 patients had solitary abscesses, and
reviewing CEUS images. Each reader was trained for scoring TSE 2 patients had 3 abscesses each. Six patients underwent percutane-
and used a subjective 5-grade scale to identify diagnostic confi- ous drainage procedures of their abscesses and antibiotic treat-
dence (grade 1 = TSE was definitely not present, grade 2 = proba- ment. One patient underwent partial hepatic resection. The other
bly not present, grade 3 = indeterminate likelihood of TSE, grade 31 patients were treated conservatively with antibiotics.
4 = probably present, and grade 5 = definitely present). Two
readers individually reviewed the same CEUS images, and each
made his own TSE scores. The results of the reading were re- CT Imaging Results
corded on a data sheet, which included lesion number and size, in- Dynamic CT imaging revealed 42 intrahepatic abscesses in
dependent diagnostic grade, and location with respect to liver 38 patients. Forty lesions (96%) were in the right hepatic lobe.
segment of TSE. Contrast-enhanced CT images of patients ob- The mean size of the abscess was 5.5 cm (range, 1–10 cm).
tained within 1 to 2 days before or after the CEUS examination Early-phase dynamic CT scans of 18 abscesses (43%) in
were obtained independently and retrospectively reviewed by a ra- 17 patients showed TSE surrounding the hepatic abscesses
diologist (K.S. with 3 years of experience in CT image reading) (Figs. 1A and 2A). This transient hepatic enhancement occurred
who was aware of the selection of focal liver lesion, CT diagnosis only in the liver segments that involved the abscesses and was
of the lesions, and contrast-enhanced CT imaging features of TSE. not visible on late-phase dynamic CT (Figs. 1B, 2B, 3A, and 4A).
The same 5-grade scale for TSE diagnosis was used to grade diag- In 37 abscesses (88%), early- and late-phase dynamic CT images
nostic confidence in the presence of TSE. The location, number, showed central hypodense areas in the abscess; 34 of 42 abscesses
and scale of TSE diagnosis for every focal liver lesion detected had irregularly enhancing septations (total or partial internal
by using CT were recorded on a data sheet. For TSE diagnostic honeycomb appearance) on both the early- and late-phase dynamic

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J Comput Assist Tomogr • Volume 00, Number 00, Month 2017 Segmental Enhancement of Pyogenic Liver Abscess

FIGURE 1. A representative image of a pathology-proven hepatic abscesses in a 43-year-old man. A, Early-phase (30-second) dynamic
contrast-enhanced CT scan shows the double-target sign, which consists of a central cystic area with an inner enhanced rim (arrow). Note
the wedge-shaped enhancement (arrowheads) of the hepatic parenchyma surrounding the mass. B, Late-phase (90-second) dynamic CT
scan shows thick rim enhancement (arrow). The wedge-shaped enhancement is no longer seen. C, In the early arterial phase (15 seconds),
the CPS scan with contrast-enhanced CT imaging shows a similar wedge-shaped enhancement area (arrowheads), thickened abscess wall
enhancement, and an internal liquefied cavity (arrow). D, During the late phase of US enhancement (50 seconds after injection), the
wedge-shaped enhancement observed in C has disappeared. E, This photomicrograph shows an organized abscess composed of
inflammatory cell infiltration and fibrosis. The portal tracts that surround the abscess have marked periportal inflammatory cell infiltration
and stenosis of the portal venules (hematoxylin-eosin staining, original magnification 40).

CT scans (Fig. 3A). Early- and late-phase dynamic CT scans Sonography Results
showed a relatively thick or irregular ring-like enhancement of
the intermediate and peripheral zones in 31 abscesses (74%; Contrast-enhanced US revealed 38 intrahepatic abscesses in
Fig. 1A). In the late phase, hypodense areas were observed 38 patients, with a mean size of 5.3 cm (range, 1.5–11 cm).
around 7 lesions (17%; Fig. 3C). In 16 (42%) of 38 abscesses in 16 patients, TSE was evident in
the early arterial phase of CEUS imaging, and it was located in the
Interreader Agreement segments that involved abscesses (Figs. 1C and 2C). With real-time
Interreader agreement for CEUS TSE interpretation based on CEUS, the dynamic enhancement of abscess was characterized by
a 5-grade scale was good (κ = 0.721). the rapid enhancement around the abscess during the arterial

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Sun et al J Comput Assist Tomogr • Volume 00, Number 00, Month 2017

FIGURE 2. Hepatic abscess in a 45-year-old man. A, This early-phase dynamic CT scan shows a huge right hepatic abscess with the
double-target sign (arrow) and a wide range of segmental enhancements that differ between the right and left hepatic lobes (arrowheads).
B, This late-phase (90-second) dynamic CT scan shows thick rim enhancement (arrow). The wedge-shaped enhancement is no longer seen.
The thickened abscess wall enhancement and double-target sign (arrow) become more obvious by this stage of the scanning process.
C, Contrast-enhanced US images with intercostal scanning in the early arterial phase. This CPS scan shows an internal liquefied cavity (arrow)
and segmental enhancement (arrowhead), which differ between the right and left hepatic lobes. D, Contrast-enhanced US images in the
late phase of US enhancement (50–55 seconds after injection of contrast agent) show that the wedge-shaped enhancement mentioned in
C has disappeared.

phase. This kind of imaging feature lasted until the late arterial phase. Comparison Between Contrast-Enhanced CT
In the 16 patients in whom TSE was demonstrated with CEUS, there and Sonography
was no significant difference in the degree of enhancement of Of 38 patients, 16 (42.1%) showed typical signs of TSE.
lesions in the late phase (starting from the portal enhancement) Meanwhile, the images of enhanced CT showed characteristics
compared with the enhancement of the surrounding liver of typical TSE in 18 (47.4%) of 38 patients. There were 0 cases
parenchyma (Figs. 1D and 2D). The enhancement of 5 lesions in scored to be indeterminate grade 3. These were classified as
5 patients even extended to the late phase when the enhancement non-TSE. Considering that enhanced CT was the reference stan-
of local liver segment subsided at a significantly slower rate than dard for the identification of TSE, the sensitivity and specificity
the surrounding liver. Liquefied lesions (35/38 abscesses [92.1%]) of CEUS for identifying TSE were 89% and 100%, respectively.
had an enhancing rim and a nonenhancing center. Consequently, a The positive predictive value was 100%, and the negative predic-
clear internal margin was recognizable in these lesions (Figs. 2C, tive value was 92%.
3B, and 4B). The enhancing rim varied in thickness among
abscesses (Figs. 3B and 4B). The enhancement extended to the DISCUSSION
internal septa and persisted during the later phases of CEUS Low mechanical index sonography is a recently introduced
(Figs. 3 and 4). An overall internal honeycomb appearance of the tool that allows real-time gray-scale exploration of the liver with
septa was identified by CEUS in 17 abscesses of a somewhat the administration of second-generation contrast media.1–3,10,12–16
smaller size (Figs. 2C and 3B). The local honeycomb-like Contrast-specific harmonic imaging techniques use a low applied
enhancement near the adjacent abscess walls was observed in 12 acoustic peak pressure to produce images that are based on the
lesions. Perilesional hypoechogenicity of the abscesses was nonlinear acoustic interaction between a US beam and
noted in 3 abscesses in 3 patients between 1 and 3 minutes after microbubbles in the contrast medium.12,17–19
the injection of contrast (Fig. 3D). Three abscesses had high- Several enhanced CT and CEUS features of hepatic ab-
intensity internal echoes with reverberation of the signal. scesses have been reported in the literature.1–10,20 Hepatic

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J Comput Assist Tomogr • Volume 00, Number 00, Month 2017 Segmental Enhancement of Pyogenic Liver Abscess

FIGURE 3. Hepatic abscesses in a 48-year-old woman with a 6-year history of diabetes. A, Late-phase dynamic CT imaging shows a
relatively thick and irregular ring-like enhancement of the intermediate and internal honeycomb. B, Late-arterial-phase CPS scan shows a
central anechoic abscess cavity with irregularly enhancing septa (partial internal honeycomb appearance; arrowhead). C, A CT cross section
caudal to the section shown in A shows a broader range of the hypodense area. D, Contrast pulse sequencing angiographic images using
ultrasonographic scanning over the costal margin show that the adjacent section of the abscess in A to C has a wide area of perilesional
hypoechogenicity.

abscesses are depicted as single or multiloculated hypodense TSE that surrounded the hepatic abscesses identified by contrast-
masses that frequently have a peripheral rim or capsule that is en- enhanced CT images; in 16 of these 18 patients, TSE proved by
hanced clearly with both imaging modalities. Of the 38 patients in CT was identified by CEUS. Other researchers9 have hypothesized
our study, 18 patients had segmental or wedge-shaped hepatic that this transient enhancement is a result of localized hepatic

FIGURE 4. A, Late-phase (90-second) dynamic CT scan shows a thick rim (arrowheads) and septal enhancement (arrow). B, Late-phase (50- to
55-second) CPS image shows a thick rim (arrowheads) and septal enhancement (arrow).

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Sun et al J Comput Assist Tomogr • Volume 00, Number 00, Month 2017

venous obstruction caused by the acute inflammation of the hepatic discovery of the TSE sign with CEUS could help to diagnose
parenchyma that surrounds the abscess. From findings on CT dur- liver abscesses in patients who have no significant fever or
ing arterial portography and hepatic arteriography, Gabata et al10 changes in blood parameters or in those who present with
hypothesized that a segmental or wedge-shaped enhancement re- nonspecific sepsis.
flects a decrease in blood flow in the portal venous system and a
compensatory increase in the rate of arterial blood flow. The dy-
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Copyright © 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
This paper can be cited using the date of access and the unique DOI number which can be found in the footnotes.

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