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1
Department of Radiology, Mail Code 7800, University of Texas Health Science
Center at San Antonio, 7703 Floyd Curl Dr.,, San Antonio TX 78229.
2
Present address: Department of Radiology, University of Erciyes, Kayseri,
Turkey.
3
Present address: Department of Radiology, Hanyang University Hospital, Seoul,
133-792, Korea.
Received October 31, 2000;
accepted after revision February 2, 2001.
Supported in part by a grant from RITA Medical Systems, Mountain View, CA,
which included partial salary support for H. Rhim.
Abstract
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MATERIALS AND METHODS. Twenty-five patients, 10 with hepatocellular carcinoma (HCC) and 15 patients with metastases who developed tumor recurrence after radiofrequency ablation of hepatic neoplasms, formed the study population. Three observers reviewed the CT scans of these patients and evaluated the location (local intrahepatic, remote intrahepatic, or extrahepatic) of all recurrent lesions and the morphology and enhancement characteristics of local intrahepatic recurrences.
RESULTS. Local intrahepatic recurrences were seen in nine patients (90%) and 11 patients (73%); remote intrahepatic recurrences, in five patients (50%) and seven patients (45%); and extrahepatic recurrences, in zero and six patients (40%) with recurrent HCC and recurrent metastases, respectively. Of the 12 nodules of local intrahepatic recurrences in HCC and the 24 in metastases, the patterns of local intrahepatic recurrences were of nodular, halo, and gross enlargement types in eight (67%) and nine (38%), four (33%) and six (38%), and zero and nine (37%) nodules in HCC and hepatic metastases, respectively. The number of local intrahepatic recurrent lesions enhancing in the arterial phase was significantly greater in HCC.
CONCLUSION. Tumor recurrences occurred at intra- and extrahepatic sites after radiofrequency ablation of hepatic neoplasms. The local intrahepatic recurrences appeared in three patterns: nodular, halo, or gross enlargement. The sites of recurrence and the morphologic patterns of local intrahepatic tumor recurrence differed between primary and secondary hepatic neoplasms.
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Radiofrequency Procedure
All ablations were performed with a Food and Drug Administration-approved
radiofrequency device (Model 30; RITA Medical Systems, Mountain View, CA). The
system consisted of a 50-W alternating electric-current generator, disposable
adhesive ground pad, and a unique disposable 15-gauge needle electrode. The
needle electrode had four retractable curved electrodes in its tip, the
positions of which were controlled by a plunger in the needle hub. Under
sonographic guidance, an ablation was performed by placing the tip of the
needle electrode into the tumor, advancing the curved electrodes, activating
the radiofrequency generator, and heating the target tissue to a temperature
greater than 90°C for 6 min. Each ablation created an approximate 3-cm
spherical thermal injury. Tumors measuring less than 3 cm were treated with
one or two ablations; those greater than 3 cm were treated with multiple
overlapping ablations.
Imaging Protocol
All patients were followed up with serial unenhanced and dual-phase
contrast-enhanced CT of the liver performed within 1 week, at 1 month, and
then every 3 months after the last ablation session. Images were acquired on
helical CT scanners (HiSpeed Advantage, General Electric Medical Systems,
Milwaukee, WI; or Picker PQ or PQ 5000, Picker International, Cleveland, OH)
with 1-sec rotations. Unenhanced images were contiguous axial scans obtained
in a nonhelical manner through the liver before contrast injection. Arterial
phase imaging was initiated at 25 sec, and portal venous phase imaging, at 65
sec after initiation of infusion of a 5 mL/sec injection of 150 mL of
non-ionic IV contrast material, ioversol 68% (Optiray 320; Mallinckrodt, St.
Louis, MO). IV contrast material was administered via a power injector (CT
9000; Liebel-Flarsheim, Cincinnati, OH). All scans were obtained with 7- to
8-mm collimation, 220 mA, and 120 kVp. The pitch (ranging between 1 and 1.5)
was adjusted as necessary to allow a single helical acquisition through the
entire liver in each phase. Scanning for all three phases was initiated at the
dome of the right hemidiaphragm and continued caudally through the entire
liver.
Image Analysis
One hundred and eleven CT scans were analyzed retrospectively by a
consensus of three observers, all radiologists. Differences of opinion were
resolved by majority rule. The number of follow-up CT examinations for each
nodule ranged from three to seven (mean, 4.4). Scans were evaluated in
chronologic order. The findings of each of the imaging phases of the scans
were recorded independently.
The observers evaluated each CT scan for the presence and location of intra- or extrahepatic tumor recurrence. Intrahepatic tumor recurrence was classified as local or remote. Local intrahepatic recurrence was defined as recurrence at or contiguous to the site of a prior ablation in the liver. Remote intra-hepatic recurrence was defined as the development of a new lesion in the liver at a site discontiguous to a prior ablation. Time to recurrence was recorded for each location.
The observers determined the morphologic characteristics of each local intrahepatic recurrent lesion on the basis of the development of new nodules and changes in size, sharpness of margins, and the enhancement characteristics of the ablated area.
On the basis of enhancement pattern, all types of local intrahepatic recurrence were classified as being hypervascular, hypovascular, or indiscernible relative to the enhancement of the adjacent hepatic parenchyma.
Data Analysis
The frequencies of different locations of recurrences of HCC and metastases
were compared. The various morphologic parameters were tabulated, and patterns
were sought. The differences between the morphologic and enhancement patterns
of recurrent HCC and recurrent metastases were compared. The statistical
significance of the differences was determined with the Fisher's exact test.
We compared the number of days to recurrence for each case, and we compared
those for HCC and metastases, using the Student's t test. We also
compared the number of days to local intrahepatic, remote intrahepatic, and
extrahepatic recurrence, using the Student's t test.
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Morphologic Patterns of Local Intrahepatic Recurrence
On the basis of morphologic characteristics, three patterns of local
intrahepatic recurrence emerged. We named them nodular, halo, or gross
enlargement-type patterns. The nodular-type pattern appeared as a new focal
mass abutting the margin of the ablation site and protruding either internally
or externally from the ablated tumor (Figs.
1A,1B,1C,1D,1E
and
2A,2B,2C).
The halo-type pattern appeared as a discernible rim of tissue in the margin of
a treated tumor that was of a different attenuation or degree of enhancement
than the ablated tumor or the adjacent hepatic parenchyma (Fig.
3A,3B,3C).
The gross enlargement-type pattern appeared as an increase in the overall
tumor size compared with that in the previous scan (Fig.
4A,4B,4C).
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Overall 36 tumor nodules developed local intrahepatic recurrence. Of these, 12 recurrences occurred in nine patients with HCC, and 24 occurred in 11 patients with metastases from extrahepatic malignancies. Among the 12 ablated HCC nodules that developed local intra-hepatic recurrence, the morphologic pattern was nodular type in eight (67%), halo type in four (25%), and gross enlargement type in none. Among the 24 ablated metastatic nodules from extrahepatic neoplasms that developed local intrahepatic recurrence, the morphologic pattern was nodular type or gross enlargement type in nine (38%) lesions each and halo type in six (25%). The gross enlargement-type pattern of local intrahepatic recurrence was significantly more common in patients with metastases from extrahepatic primary neoplasms, than in those with HCC (p < 0.01).
Enhancement Patterns of Local Intrahepatic Recurrence
Of the HCC recurrences, all local intrahepatic recurrent lesions,
irrespective of the morphologic type, were hypervascular in the arterial phase
(Fig. 1D). In the portal venous
phase, seven (88%) of the eight recurrent nodules
(Fig. 1E) and one (25%) of the
four halo-type lesions were indiscernible, and the remaining three (75%)
halo-type lesions were hypovascular.
Of the local intrahepatic tumor recurrences in patients with extrahepatic primary neoplasms, all nodular and gross enlargement-type and three (50%) of the six halo-type lesions were hypovascular in the arterial phase. Two (33%) of the halo-type lesions were hypervascular, and one (17%) was indiscernible in the arterial phase. In the portal venous phase, six (67%) of the nine nodular type, all halo type, and five (56%) of the nine gross enlargement-type lesions were hypovascular. Two (22%) nodular type and four (44%) gross enlargement-type lesions were hypovascular with a hypervascular rim. The remaining one nodular-type marginal lesion from the only patient with metastases from breast cancer was hypervascular in the portal venous phase. The difference in the attenuation characteristics of the lesions in the recurrent HCC and the recurrent metastases groups in the arterial phase was statistically significant (p < 0.005).
In all cases of HCC or metastases, the hypervascular type of local intrahepatic recurrences were different from the usual postablation peritumoral hyperemia in that the zone of hyperemia either increased or recurred after having faded away in the course of the disease.
Of the six patients with metastases from extrahepatic primary neoplasms who had extrahepatic recurrence, the extrahepatic lesions were in the peritoneum in three (50%), lungs in two (33%), and regional lymph nodes in one patient (17%).
Temporal Course of Postablation Tumor Recurrence
In the 10 patients with recurrent HCC, local recurrence occurred from 30 to
420 days (mean, 167 days) after ablation. Remote intrahepatic lesions were
seen between 99 and 420 days (mean, 233 days). No extrahepatic lesions were
identified during the time frame of this study.
In the 15 patients with recurrent metastases, local recurrence occurred from 30 to 362 days (mean, 157 days) after ablation. New intrahepatic (remote) lesions were seen between 79 and 256 days (mean, 132 days). The six extrahepatic metastases were identified between 57 and 362 days (mean, 233 days) after the ablation of the initial liver lesion. The time to intrahepatic recurrence was not significantly different between the HCC and the metastases groups.
In both groups, the times to local and remote intrahepatic recurrence were not significantly different. The time to extrahepatic recurrence in patients with metastases was significantly higher than the time to intrahepatic recurrence (p < 0.03).
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Our data suggest that recurrence of HCC has features that are significantly different from those of metastases after ablation. First, extrahepatic recurrences (in the lungs, lymph nodes, and peritoneum at the site of previous surgery for colon cancer) were significantly more common in patients with extrahepatic primary neoplasms than in those with HCC. Second, the most common pattern of local intrahepatic recurrence in patients with HCC was nodular (67%), followed by halo-type pattern (33%). All lesions were hypervascular on the arterial phase images, but 66% were indiscernible on the portal venous phase images. On the other hand, after ablation of metastatic lesions from extrahepatic primary neoplasms, the local recurrence pattern of gross enlargement type was as common as the nodular type (37% each). Twenty-six percent of the local recurrences in the metastatic group showed the halo-type pattern. All lesions were hypovascular in both the arterial and the portal venous phases. In only the one patient with metastases from primary breast carcinoma did the recurrent lesions enhance in both phases.
The differences between the recurrent hepatic lesions of HCC and those of metastases from extrahepatic primary neoplasms are to be expected and reflect the differences in the natural history and imaging findings of these neoplasms described in the literature. Two studies have shown extrahepatic metastases to be rare in patients with intrahepatic stage I and stage II neoplasms [21, 22]. However, in patients who had advanced HCC, Ferris et al. [21] and Katyal et al. [22] found extrahepatic recurrence commonly seen in lungs, lymph nodes, adrenals, and bones. In our series, most patients had stage I or stage II tumors. Of the patients who had stage IV tumors, none had vascular invasion. In our opinion, this finding explains the absence of metastases in our HCC population. On the other hand, patients with extrahepatic primary neoplasms who had liver metastases were already staged as M1 by the TNM classification. Therefore, some patients developed additional extrahepatic lesions.
In the past, various studies have shown the differences between the enhancement pattern of HCC and that of hepatic metastases from extrahepatic primary neoplasms. HCC is typically hypervascular in the arterial phase and may become isodense compared with the adjacent uninvolved liver parenchyma in the portal venous phase [23,24,25,26,27,28]. On the other hand, the CT features of liver metastases depend on the primary neoplasm. Metastases from most primary neoplasms are hypovascular in both arterial and portal venous phases [13, 28, 29]. Some primary neoplasms, for example carcinoid, thyroid carcinoma, renal cell carcinoma, and some breast cancers, show metastases that are hypervascular and may show up better on the arterial than on the portal venous phase [13, 30].
Based on the observed significant difference between the patterns of recurrent HCC and recurrent metastases, our findings have some important clinical implications that we have incorporated into our clinical practice. In patients with ablated HCC, images obtained in the arterial phase after a power injection of an adequate amount of contrast agent at 5 mL/sec are critical in depicting small tumor nodules, which are visible only on the arterial phase. However, arterial phase images do not provide any additional information in patients with recurrent metastases from extrahepatic malignancies and need not be obtained routinely. Second, the low-attenuation recurrent metastatic lesions contiguous with the low-attenuation ablated area may be subtle enough to be recognizable only by detecting a change in the size, margins, or configuration of the existing area of ablation. During the interpretation of scans, the reviewer must compare the ablated lesions with the previous scans to look for any subtle changes. Therefore, a baseline scan is important. If present, subtle changes should be correlated with tumor markers to assess their significance. Elevated tumor markers with no evidence of intrahepatic recurrence should lead to a search for extrahepatic recurrences. Third, after ablation of hepatic metastases from colon cancer, follow-up CT must include the pelvis for early detection of local recurrences at the colectomy site and regional lymph node recurrences. It is probably reasonable to perform chest CT every 6 months in these patients. On the other hand, in patients with HCC, pelvis and chest CT need not be included in the routine follow-up CT protocol. Fourth, each CT scan must be closely scrutinized in its entirety because there is a natural tendency to concentrate on the ablation site and ignore the rest of the liver and extrahepatic sites. In our own practice, ignoring these sites has resulted in a delayed detection of both remote intrahepatic and extrahepatic tumor recurrence. Last, a large range of time to tumor recurrences extends up to 420 days and perhaps beyond. Therefore, an adequate length of follow-up is required before ablation can be considered curative in any given patient.
The main limitation of our study is that we have reported only recurrences that were seen on CT. The complete extent and distribution of recurrence after ablation is still unknown.
In conclusion, our data suggest that tumor recurrences are primarily intrahepatic in patients with ablated HCC and both intra- and extrahepatic in patients with ablated metastases. The CT pattern of tumor recurrence ranges from subtle to obvious. High-quality appropriately protocolled CT and familiarity with the spectrum of imaging findings will facilitate early detection and the potential for retreatment of recurrent tumor in patients treated with radiofrequency thermal ablation.
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1.5 cm) malignant hepatic neoplasms.
AJR
1995;164:879
-884
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