DOI:10.2214/AJR.04.1932
AJR 2006; 187:W341-W349
© American Roentgen Ray Society
Imaging Features of Hepatocellular Carcinoma After Transcatheter Arterial Chemoembolization and Radiofrequency Ablation
Hyo Soon Lim1,
Yong Yeon Jeong1,
Heoung Keun Kang1,
Jae Kyu Kim2 and
Jin Gyoon Park2
1 Department of Diagnostic Radiology, Chonnam National University Medical School
and Chonnam National University Hwasun Hospital, 160 Ilsim-ri, Hwasun-eup,
Hwasun-gun, Jeollanam-do 519-809, South Korea.
2 Department of Diagnostic Radiology, Chonnam National University Medical School
and Chonnam National University Hospital, Gwangju, South Korea.
Received December 20, 2004;
accepted after revision August 8, 2005.
Address correspondence to Y. Y. Jeong
(yjeong{at}chonnam.ac.kr).
WEB
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Abstract
OBJECTIVE. The purpose of this pictorial essay is to show the
imaging features of hepatocellular carcinoma (HCC) after transcatheter
arterial chemoembolization (TACE) and radiofrequency thermal ablation on CT,
MRI, and contrast-enhanced sonography and to describe the advantages and
limitations of each imaging technique in evaluating the therapeutic effect on
HCC.
CONCLUSION. CT is the standard imaging technique for monitoring the
effectiveness of TACE and radiofrequency ablation. Contrast-enhanced
sonography and MRI can complement CT in evaluating the therapeutic
response.
Keywords: CT • hepatocellular carcinoma • liver disease • MRI • radiofrequency ablation • sonography • transcatheter arterial chemoembolization
Introduction
Although surgery remains the treatment of choice for hepatocellular
carcinoma (HCC), several minimally invasive techniques have been used as
alternatives to surgery for treating the disease. These include transcatheter
arterial chemoembolization (TACE) and percutaneous therapy, such as
percutaneous ethanol injection therapy, percutaneous microwave coagulation
therapy, and radiofrequency ablation therapy
[1]. Although several
therapeutic options have been advocated, the most widely used are TACE,
radiofrequency ablation, or a combination of the two. After treatment,
follow-up imaging studies, including CT, MRI, and contrast-enhanced
sonography, have been used to assess the therapeutic efficacy. The purpose of
this pictorial assay is to show the imaging features of HCC after TACE and
radiofrequency ablation.
Transcatheter Arterial Chemoembolization
TACE, using iodized oil mixed with anticancer agents, has been widely used.
Iodized oil is used as a vehicle to transport the anticancer drug, and the
embolic material enhances the antitumor effect of the anticancer drug
[2]. TACE causes acute ischemic
damage to the HCC and results in coagulative necrosis because HCC is nourished
only by the hepatic artery.
CT and MRI
CT is commonly used as the standard imaging technique for evaluating the
therapeutic response in patients with HCC after TACE. The accumulation pattern
of iodized oil observed on CT can be classified into four types: type I,
homogeneous accumulation, with type Ia indicating accumulation around the
tumor and type Ib indicating no accumulation around the tumor; type II,
partial defect in the tumor; type III, faint accumulation; and type IV, no or
slight accumulation [3] (Figs.
1A,
1B,
1C,
1D, and
1E). The pattern and
distribution of iodized oil in the tumor are useful for assessing the
therapeutic effects of TACE. A greater amount of accumulation of iodized oil
within tumor indicates a greater area of necrosis. During follow-up, the focal
defect or washout of iodized oil in the mass with the contrast-enhanced area
suggests the presence of a viable tumor and that additional treatment is
needed [4] (Figs.
2A,
2B, and
2C).
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Fig. 1A —Four types (with type I broken down into two parts) of
accumulation patterns of iodized oil on CT after transcatheter arterial
chemoembolization. Greater amount of accumulation of iodized oil within tumor
indicates greater area of necrosis. Type Ia, seen in 60-year-old man, has
homogeneous accumulation, with accumulation also seen around tumor.
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Fig. 1B —Four types (with type I broken down into two parts) of
accumulation patterns of iodized oil on CT after transcatheter arterial
chemoembolization. Greater amount of accumulation of iodized oil within tumor
indicates greater area of necrosis. Type Ib, seen in 59-year-old man, has
homogeneous accumulation with accumulation not seen around tumor.
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Fig. 1C —Four types (with type I broken down into two parts) of
accumulation patterns of iodized oil on CT after transcatheter arterial
chemoembolization. Greater amount of accumulation of iodized oil within tumor
indicates greater area of necrosis. Type II, seen in 73-year-old man, has
partial defect in accumulation.
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Fig. 1D —Four types (with type I broken down into two parts) of
accumulation patterns of iodized oil on CT after transcatheter arterial
chemoembolization. Greater amount of accumulation of iodized oil within tumor
indicates greater area of necrosis. Type III, seen in 65-year-old woman, has
faint accumulation.
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Fig. 1E —Four types (with type I broken down into two parts) of
accumulation patterns of iodized oil on CT after transcatheter arterial
chemoembolization. Greater amount of accumulation of iodized oil within tumor
indicates greater area of necrosis. Type IV, seen in 70-year-old man, has no
or slight accumulation.
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Fig. 2A —56-year-old man with residual viable tumor that shows faint
accumulation of iodized oil after transcatheter arterial chemoembolization
(TACE). On follow-up unenhanced CT scan 3 weeks after TACE, faint accumulation
of iodized oil (arrow) within tumor is seen.
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Fig. 2B —56-year-old man with residual viable tumor that shows faint
accumulation of iodized oil after transcatheter arterial chemoembolization
(TACE). Arterial phase CT scan shows contrast enhancement (arrow)
around faint accumulation of iodized oil, suggesting remaining viable
tumor.
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Fig. 2C —56-year-old man with residual viable tumor that shows faint
accumulation of iodized oil after transcatheter arterial chemoembolization
(TACE). Subsequent angiogram shows hypervascular mass (arrows) in
hepatic dome. Because of this finding, TACE was repeated.
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Necrotic tissue on contrast-enhanced CT and MRI does not show contrast
enhancement, whereas enhancement is observed in residual tumor (Figs.
3A and
3B). It can be difficult to
evaluate contrast enhancement in a tumor with partial retention of iodized oil
on contrast-enhanced CT because of the beam-hardening artifacts produced by
the high attenuation of iodized oil. The signal intensity of MRI is not
influenced by the presence of iodized oil; therefore, a residual viable tumor
is better defined by contrast-enhanced MRI
[5] (Figs.
4A,
4B,
4C,
4D,
4E, and
4F). Even though MR images
have much better contrast resolution, it is difficult to detect the small
residual areas of viable cells seen microscopically in the capsule because the
capsule appears as a hyper-intense ring in the early and late phases of
dynamic enhancement [6].
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Fig. 3A —54-year-old man with residual viable tumor with defective
accumulation of iodized oil after transcatheter arterial chemoembolization
(TACE). On unenhanced CT scan 3 weeks after TACE, defective accumulation of
iodized oil (arrows) within tumor is seen.
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Fig. 3B —54-year-old man with residual viable tumor with defective
accumulation of iodized oil after transcatheter arterial chemoembolization
(TACE). Arterial phase CT scan shows contrast enhancement (arrows)
within defective uptake of iodized oil, suggesting remaining viable tumor.
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Fig. 4A —66-year-old woman with residual viable tumor after
transcatheter arterial chemoembolization. On unenhanced CT scan, dense
intratumoral retention of iodized oil (arrow) is shown with
beam-hardening artifact.
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Fig. 4C —66-year-old woman with residual viable tumor after
transcatheter arterial chemoembolization. Axial T1-weighted gradient-echo
(TR/TE, 120/4.2) MR image shows hyperintense lesion (arrow).
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Fig. 4D —66-year-old woman with residual viable tumor after
transcatheter arterial chemoembolization. Axial T2-weighted single-shot fast
spin-echo (infinite/92) MR image shows heterogeneous hyperintense lesion.
Necrotic lesions (arrowheads) have higher signal intensity than do
viable lesions (arrow).
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Fig. 4E —66-year-old woman with residual viable tumor after
transcatheter arterial chemoembolization. On gradient-echo (180/1.8)
T1-weighted MR images after administration of gadolinium chelates, residual
viable tumor (arrow) shows intense enhancement in arterial phase
(E) and washout in delayed phase (F). Necrotic lesion
(arrowheads) shows no enhancement in either phase.
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Fig. 4F —66-year-old woman with residual viable tumor after
transcatheter arterial chemoembolization. On gradient-echo (180/1.8)
T1-weighted MR images after administration of gadolinium chelates, residual
viable tumor (arrow) shows intense enhancement in arterial phase
(E) and washout in delayed phase (F). Necrotic lesion
(arrowheads) shows no enhancement in either phase.
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HCC after TACE has variable signal intensity on T1- and T2-weighted images.
The hypointensity on T2-weighted images represents coagulation necrosis (Figs.
5A and
5B). Conversely, the
hyperintensity corresponds to hemorrhage or residual tumor
[6]. However, it is sometimes
difficult to distinguish a viable tumor from necrotic areas on T1- and
T2-weighted images.
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Fig. 5A —64-year-old man with complete necrosis of hepatocellular
carcinoma after transcatheter arterial chemoembolization. Axial T1-weighted
gradient-echo (TR/TE, 120/4.2) MR image shows hyperintense lesion
(arrow).
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Fig. 5B —64-year-old man with complete necrosis of hepatocellular
carcinoma after transcatheter arterial chemoembolization. Axial T2-weighted
single-shot fast spin-echo (infinite/92) MR image shows hypointense lesion
(arrow), which represents coagulation necrosis. Compact uptake of
iodized oil is seen within tumor on CT (not shown).
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Sonography
Contrast-enhanced sonography using a microbubble contrast agent may be
useful for detecting residual or recurrent tumors in HCC after TACE
[7]. The blood flow signals are
detected within the residual viable tumor (Figs.
6A,
6B, and
6C); however, a reliable
assessment of intratumoral blood flow may not be possible in many instances,
particularly in small lesions or in lesions located deep within the liver
parenchyma [6,
7].
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Fig. 6A —74-year-old man with incomplete necrosis of hepatocellular
carcinoma after transcatheter arterial chemoembolization (TACE). On follow-up
unenhanced CT scan 3 weeks after TACE, defective accumulation of iodized oil
(arrow) within tumor is seen.
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Fig. 6B —74-year-old man with incomplete necrosis of hepatocellular
carcinoma after transcatheter arterial chemoembolization (TACE). Arterial
phase CT scan shows contrast enhancement (arrow) within lesion.
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Fig. 6C —74-year-old man with incomplete necrosis of hepatocellular
carcinoma after transcatheter arterial chemoembolization (TACE).
Contrast-enhanced sonography clearly shows enhancement of lesion
(arrows) irrespective of accumulation of iodized oil on CT.
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Radiofrequency Ablation
Radiofrequency ablation is designed to destroy tumors by heating tissue to
temperatures exceeding 60°C. A radiofrequency current is emitted from an
electrode that is inserted during either an open surgical or a percutaneous
procedure with imaging guidance such as sonography or CT. Radiofrequency
ablation, which results in coagulation tumor necrosis, has been introduced as
a promising therapeutic technique in the treatment of small HCC
[8,
9].
CT and MRI
Complete tumor necrosis is considered to have occurred when follow-up CT or
MRI shows the absence of contrast enhancement within an ablated lesion or at
its periphery [9] (Figs.
7A,
7B,
7C, and
7D). Any focal and nodular
peripheral enhancement in the ablated lesion should be considered indicative
of residual or recurrent tumor
[10] (Figs.
8A and
8B).
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Fig. 7B —70-year-old man with successful radiofrequency ablation.
Axial T1-weighted gradient-echo (TR/TE, 180/1.8) MR image 2 months after
radiofrequency ablation shows oval ablated lesion (arrow) with high
signal intensity relative to surrounding liver parenchyma.
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Fig. 7C —70-year-old man with successful radiofrequency ablation.
Axial T2-weighted fast spin-echo (7,500/90) MR image shows oval ablated lesion
(arrow) with low signal intensity relative to surrounding liver
parenchyma, representing coagulative necrosis. Note high-signal-intensity rim
(arrowheads) representing reactive change.
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Fig. 7D —70-year-old man with successful radiofrequency ablation. On
T1-weighted MR image after administration of gadolinium chelates, ablated
lesion (arrow) shows lack of enhancement, although high signal
intensity on unenhanced MR image interferes with proper evaluation of arterial
phase enhancement.
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Fig. 8A —62-year-old man with residual tumor after radiofrequency
ablation. On follow-up CT scan 2 months after radiofrequency ablation,
arterial phase CT scan shows nodular enhancement (arrowheads) at
anterior aspect of ablated lesion (arrow).
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Fig. 8B —62-year-old man with residual tumor after radiofrequency
ablation. Delayed phase CT scan shows washout of nodular enhancement
(arrowhead) around ablated lesion (arrow). Nodule was
thought to represent residual viable tumor and was treated with repeat
radiofrequency ablation.
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Occasionally, peripheral rim enhancement resulting from reactive hyperemia
is seen at immediate follow-up imaging that is usually uniform in thickness
and resolves at follow-up CT
[9]. In successful treatment,
long-term follow-up CT shows no change or a gradual decrease in the volume of
the ablated lesion without contrast enhancement
[10] (Figs.
9A and
9B).
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Fig. 9A —55-year-old man with successful radiofrequency ablation.
Arterial phase CT scan 1 day after radiofrequency ablation shows oval-shaped
ablated lesion (arrow) with surrounding hyperemia
(arrowheads).
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Unenhanced T1- and T2-weighted MRI after radiofrequency ablation reveals
markedly heterogeneous signal intensity within the ablated lesion. This
variability in signal intensity throughout the ablated region is most likely
caused by an uneven evolution of the necrotic area and the host response to
thermal damage [11].
Therefore, for the evaluation of therapeutic response, the use of a
contrast-enhanced study is recommended, and moderate hyperintensity on
T2-weighted images associated with corresponding enhancement on
contrast-enhanced T1-weighted images offers optimal specificity for detecting
residual viable tumor (Figs.
10A,
10B, and
10C).
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Fig. 10A —80-year-old man with residual viable tumor after
radiofrequency ablation. Axial T1-weighted gradient-echo (TR/TE, 180/4.2) MR
image 2 months after radiofrequency ablation shows hypointense lesion
(arrow).
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Fig. 10B —80-year-old man with residual viable tumor after
radiofrequency ablation. Axial T2-weighted fast spin-echo (500/91) MR image
shows hyperintense lesion (arrow) that represents viable tumor.
Bright signal intensity is seen in peripheral portion (arrowhead) of
ablated lesion, representing necrosis.
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Fig. 10C —80-year-old man with residual viable tumor after
radiofrequency ablation. On axial T1-weighted MR image after administration of
gadolinium chelates, ablated lesion (arrow) shows peripheral area of
enhancement (arrowheads), suggesting residual viable tumor.
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Sonography
Contrast-enhanced sonography can be useful in detecting residual or
recurrent tumors after radiofrequency ablation of HCC (Figs.
11A and
11B). Real-time guidance of
the placement of the electrode is another useful feature of contrast-enhanced
sonography. However, the technique has some limitations in assessing the
therapeutic effect of radiofrequency ablation. Typically, well-differentiated
HCC may not show distinct intratumoral enhancement on contrast-enhanced
sonography, and HCC located in the hepatic dome is difficult to explore.
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Fig. 11A —73-year-old man with marginal recurrent tumor after
radiofrequency ablation. Follow-up CT scan 8 months after radiofrequency
ablation shows small enhancing nodule (arrowheads) at posterior
aspect of ablated lesion (arrow), representing marginal recurrent
tumor.
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Fig. 11B —73-year-old man with marginal recurrent tumor after
radiofrequency ablation. Contrast-enhanced sonography also shows focal flow
signals (arrowheads) that represent recurrent tumor vessels within
ablated area (arrow). Recurred tumor was treated with repeat
radiofrequency ablation.
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Conclusion
Evaluation of the therapeutic effect of HCC after TACE and radiofrequency
ablation is primarily based on the findings of imaging studies. CT is the
standard imaging technique for monitoring the effectiveness of TACE and
radiofrequency ablation. Contrast-enhanced sonography and MRI can complement
CT in the evaluation of the therapeutic response. To know the advantages and
limitations of each imaging technique in the evaluation of the therapeutic
effect of HCC is important in determining if the treated tumor is completely
necrotic or requires additional treatment.
Acknowledgments
We thank Bonnie Hami for her editorial assistance in the preparation of
this manuscript.
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Abstract
Introduction
