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Original Research |
1 All authors: Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Kangnam-ku, Seoul 135-710, South Korea.
Received July 19, 2004; accepted after revision October 6, 2004.
Address correspondence to S. H. Kim.
OBJECTIVE. The purpose of this study was to evaluate the doubling time, frequency, and features on dynamic CT of extrahepatic needle tract implantation of malignant neoplasms after sonographically guided percutaneous biopsy for hepatocellular carcinoma (HCC).
MATERIALS AND METHODS. Between January 1997 and June 2003, 1,055 patients underwent sonographically guided percutaneous biopsy for HCC. The serial changes of implanted tumor volume were estimated on retrospective review of CT, and their doubling times were calculated from the two CT scans showing the first and last visible implanted tumors. The frequency of extrahepatic needle tract implantation of malignant neoplasms was evaluated overall and according to the type of needle used. The CT features of the implanted tumors were examined with regard to size, number, location, morphology, and enhancement pattern.
RESULTS. The mean doubling time of extrahepatic needle tract implantation of malignant neoplasms after sonographically guided percutaneous biopsy was 112 days (range, 22–415 days). The mean time interval between biopsy and the emergence of the implanted tumor on CT was 267 days (range, 116–619 days). The overall frequency was 0.76% (8/1,055). The frequencies according to the type of needle were 1.3% (8/622) for the group treated with the end-cutting needle and 0% (0/433) for the group treated with the tru-cut needle; these frequencies differ from each other with statistical significance (p < 0.05, Fisher's exact test). Fifteen of the 17 implanted tumors were round or oval enhancing nodules along the needle tract, and 13 showed persistent enhancement on equilibrium phase images.
CONCLUSION. The doubling times of extrahepatic needle tract implantation of malignant neoplasms after sonographically guided percutaneous biopsy for HCC were similar to those of typical HCCs in the liver on CT-based analysis. The frequency was relatively low, and their CT features were similar to those reported previously.
Despite the recent advances in cross-sectional imaging techniques, imaging findings of hepatocellular carcinoma (HCC) are frequently nonspecific and confusing, so the biopsy procedure still plays an important role in determining a treatment plan. Sonographically guided percutaneous biopsy has been regarded as an effective, safe, and high-yield method for tissue diagnosis of focal hepatic lesions including HCC. However, several reports have revealed that this procedure is associated with a mortality rate of 0.006–0.031% and that 0.05–0.18% of the patients who undergo this procedure develop various complications such as hematoma; hemoperitoneum; hepatic arterial pseudoaneurysm; bile peritonitis; pneumothorax; local infection; and, rarely, anaphylactic shock [1–3].
Moreover, although the number is small, this procedure may be followed by implantation of a malignant neoplasm along the biopsy needle tract [4–13]. Several cases of needle tract implantation of a malignant neoplasm after sonographically guided percutaneous biopsy of HCC have been reported [5–10], and some investigators have reported the frequency to be 2.1–5.1% [11–13].
Although several investigations have analyzed CT findings of needle tract implantation after sonographically guided percutaneous biopsy of HCC [4, 13], to our knowledge, none has described the serial changes of implanted tumor volume and their doubling time on multiphase CT.
This study was performed to estimate the growth rate of malignant neoplasms by calculating doubling time from the serial changes of implanted tumor volume and to evaluate their frequency and dynamic CT features.
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Subjects
Over 6.5 years, from January 1997 to June 2003, 1,055 patients with HCC
underwent sonographically guided percutaneous biopsy, and the findings were
confirmed at histologic examination. Written informed consent for both
research and biopsy was obtained from all patients at the time of procedure.
However, our institutional review board did not require its approval for this
retrospective study.
A computer-based search of all medical records and radiology reports was done using the keywords "tract," "seeding," or "implant-." Included were patients with a discernible soft-tissue lesion of different attenuation from that of the surrounding tissue and at the same recorded area of biopsy in the anterior or lateral, abdominal or chest wall. Excluded were patients with a history of another percutaneous interventional procedure such as percutaneous ethanol injection therapy or percutaneous radiofrequency ablation for HCC during the follow-up period. Because we could not determine whether intrahepatic tumors were implanted or newly developed, we included only extrahepatic tumors that developed along the needle tracts in the study group.
Only eight patients had extrahepatic needle tract implantation: six men and two women who ranged in age from 44 to 66 years (mean, 55 years). A total of 17 implanted tumors were detected in these eight patients, all of which were removed successfully by surgical excision and found to be metastatic HCCs on pathologic examination.
Biopsy Technique
Percutaneous biopsy of HCC in the liver was done under the guidance of
real-time sonography with the freehand technique. Two kinds of biopsy needles
were used: end-cutting (AutoVac, Angiomed) and tru-cut (Gunbiopsy Needle,
M.I.Tech), both of which are spring-loaded and fully automated.
The outer diameters of the end-cutting and tru-cut needles were 19.5- and 18-gauge, respectively. The mechanism of harvesting tissue with an end-cutting needle is to take out the tissue cut by and within a simple cylindrical needle. In case of a tru-cut needle, the mechanism is to harvest the trapped tissue in the groove of a stylet after shooting a cylindrical cuff. Percutaneous biopsy was performed using end-cutting needles in 622 patients and tru-cut needles in 433 patients. None of the patients in our study group was biopsied with both types of needle for a histologically confirmed HCC. Fisher's exact test was used to analyze the difference in the frequencies of needle tract implantation between the two groups.
CT Technique
All eight patients were followed up with triple-phase helical CT on one of
three randomly selected CT scanners (HiSpeed, LightSpeed QX/i, or LightSpeed
Ultra; GE Healthcare). The helical CT images were obtained in a craniocaudal
direction from the top of the liver to the level of the lower pole of the
right kidney, with 2.5- to 7.5-mm reconstruction interval and 5- to 7.5-mm
slice thickness. A 100-mL dose of 60% nonionic contrast material (Ultravist
300 [iopromide], Schering) was administrated at a rate of 3 mL/sec using an
automated power injector (OP 100, Medrad). Images were obtained before
contrast medium injection and 30, 60, and 180 sec after the initiation of IV
injection of contrast medium, representing the hepatic arterial, portal
venous, and equilibrium phases, respectively. Unenhanced images were
unavailable in two patients.
CT Analysis
Two radiologists reviewed all the phases of initial and follow-up CT
examinations retrospectively and by consensus. The volumes of all implanted
tumors were measured by integrating the tumor areas of all slices on arterial
phase images of all follow-up CT (adding the products of slice thickness and a
tumor area on the slice). In this way, the serial changes of tumor volume were
estimated. To compare with the previously reported growth rate of intrahepatic
HCC, the doubling time (DT) of each extrahepatic implantation tumor
was calculated from the two CT scans showing the first and last visible
implanted tumors using of the following exponential and logarithmic function
[14]:
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The time interval between the date of biopsy and emergence of the first implanted tumor was estimated on retrospective review of CT examinations in each patient. The frequency of needle-tract implantation was analyzed in total and according to the needle type used.
Implanted tumors were investigated in terms of number, size, and location on all follow-up CT images from emergence of the first implanted tumor to removal, and morphology and enhancement pattern were recorded using the latest CT examination before removal. Homogeneity of enhancement of the implanted tumors was evaluated on arterial phase images. Dynamic changes of all implanted tumors during the three phases after IV contrast material injection were evaluated in two ways: first, visual estimation, in which the attenuation of each implanted tumor was categorized as high, iso-, or low compared with that of the adjacent intercostal muscle during the same phase; and, second, attenuation measurements on all phases. Arterial enhancement was defined as when the attenuation measurement of the implanted tumor on the arterial phase image increased by 20 H or more compared with that of the implanted tumor on the unenhanced image. Delayed washout was defined as when the attenuation measurement of the implanted tumor on the equilibrium phase image decreased by 10 H or more compared with that of the implanted tumor on the arterial phase image. When no such decrease was detected on the equilibrium phase image, we defined it as persistent enhancement. When measuring attenuation of the small implanted tumors, we tried to exclude the effect of partial-volume averaging in the peripheral portions because they were located in various environments, including areas of high attenuation such as intercostal muscles and ribs and those of low attenuation such as subcutaneous fat.
Results
Tumor Growth
The doubling time of 17 implanted tumors after sonographically guided
percutaneous biopsy for HCC, calculated from the data of tumor volume acquired
through slice integration, ranged from 22 to 415 days (mean, 112 days; median,
78 days) (Fig. 1A,
1B). These results are similar
to the previously reported data of HCCs in the liver
[15–19].
The time intervals between the dates of biopsy and emergence of the first implanted tumor on retrospective review of CT scans of the eight patients ranged from 116 to 619 days (mean, 267 days; median, 188 days). The mean volume change of each tumor ranged from 26 to 1,596 mm3 per month (mean, 469 mm3 per month). These wide ranges show their diverse properties of growth rate.
Frequencies
The frequency of extrahepatic needle tract implantation after
sonographically guided percutaneous biopsy for HCC was 0.76% (8/1,055). A
total of 17 implanted tumors were found, all of which occurred with a
frequency of 1.3% (8/622) in only those patients treated using the end-cutting
needle. None of the patients in the tru-cut needle group developed an
implanted tumor (0/433). This difference in the frequencies between the two
needle groups is statistically significant (p < 0.05, Fisher's
exact test). The mean number of needle passes was 2.87 ± 0.36 (±
SD) in the end-cutting needle group and 2.94 ± 0.31 in the tru-cut
needle group.
CT Features
A total of 17 implanted tumors were found along the needle tracts of
sonographically guided percutaneous biopsy. The longest diameters of the
implanted tumors were not more than 3.2 cm. Nine of 17 tumors were 1–2
cm (Table 1). Three patients
had one implanted tumor, another three had two, and the other two had four.
The average number of implanted tumors was 2.1 (17/8).
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Six tumors were located in the subcutaneous tissue, and another six were in the intercostal muscles. Three tumors were found in the peritoneal cavity. Two patients had a continuous or elongated lesion: from the subcutaneous tissue to the intraperitoneum in one and from the subcutaneous tissue to the intercostal muscle in the other (Fig. 2A, 2B). The other 15 tumors showed oval or round configuration with close attachment or occasional conglomeration (Fig. 3A, 3B).
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Knowing the growth pattern of implanted tumors along the needle tract after sonographically guided percutaneous biopsy for HCC is important for differentiating them from postoperative changes, such as scar or granulation tissue, and successfully managing the lesion by surgical excision.
The doubling time, a measurable factor of growth rate, of HCC in the liver has been reported several times: 29–398 days (mean, 136 days) by Sheu et al. [15], 195 days (mean) by Ebara et al. [16], 41–305 days (mean, 102 days) by Okazaki et al. [17], and 27–605 days (mean, 204 days) by Barbara et al. [18]. Kubota et al. [19] reported the doubling time of small HCCs is 35–496 days (mean, 114 days) using dynamic CT [19]. However, to our knowledge, there has been no study about the doubling time of tumors implanted along the needle tract after sonographically guided percutaneous biopsy of HCC. Our study showed radiologically that the doubling time of these implanted tumors is 22–415 days (mean, 112 days; median, 78 days). The range and mean of the doubling times of our study are similar to the results of other investigators of HCCs in the liver. These results suggest that the growth rate of the extrahepatic implanted tumor of HCC is similar to that of the intrahepatic HCC.
From a clinical point of view, knowing the time interval between biopsy and the emergence of the first implanted tumor on retrospective review of CT may be more efficacious than knowing the doubling time. However, those results seem variable. Our study showed these data to range from 116 to 619 days. Takamori et al. [12] reported that the time interval between biopsy and the detection of implanted tumors ranged from 3 months to 4 years. Although other factors may contribute to this time interval, the initial number of spilled tumor cells, the doubling time, and the microenvironment surrounding them, such as local blood supply, are important and could explain this wide range in the time interval and the serial changes of tumor volume.
In some studies, researchers have investigated the frequency of implanted tumors along the needle tract after sonographically guided percutaneous biopsy of HCC. Huang et al. [11] found implanted HCCs along the needle tract in nine (2.1%) of 420 patients. They reported four (3.2%) of 126 patients who underwent biopsy with Vim-Silverman needles and five (1.5%) of 329 patients with disposable Tru-Cut needles (Top Corporation) had implantations [11]. Takamori et al. [12] and Kim et al. [13] reported implanted tumors in three (5.1%) of 59 patients who were treated with an unknown type of needle and seven (3.4%) of 205 who were treated with an end-cutting needle, respectively. The frequency rate of 2.1–5.1% is a significant risk for routine practice. Our study showed an overall frequency of 0.76%, which is tolerable. The higher frequency of implanted tumors in the end-cutting needle group than in the tru-cut needle group is similar to the results of Huang et al. Our results suggest that the mechanism of harvesting tissue may be an important factor in tumor cell spillage and, thereafter, in implantation.
Besides the needle type, other factors of needle tract implantation such as the number of needle passes, intrahepatic length of needle tract, and pathologic grade of HCC are important. Our results showed no significant difference between the number of needle passes in each group. The penetrated original intrahepatic tumors were grouped central and peripheral, according to their outer margin in the liver, as an indirect marker of the intrahepatic length of the needle tract. If shedding of malignant cells during removal of the needle occurred near the original tumors, the original tumors with peripheral location would have more extrahepatic implantation tumors than the central tumors. Six of the eight original tumors were peripheral, which may support this hypothesis.
The morphologic characteristics of extrahepatic implantation tumors after sonographically guided percutaneous biopsy are a few small round or oval nodules with or without linear arrangement in the subcutaneous fat or intercostal muscle layers (Table 1). Although the linear arrangement pattern tells us the mechanism of implantation, it cannot always be observed because multiple needle passes are used and because of the close attachment and occasional conglomeration of the implanted tumors. According to the literature review of needle tract implantation of HCC by Takamori et al. [12], the largest diameter of the implanted tumor was 6.0 cm, but all the others were 3.5 cm or smaller [12]. In our study, the largest implanted tumor measured 3.2 cm, which is relatively small. We believe this may be the result of earlier detection of abdominal or chest wall masses using periodic CT or sonography follow-up.
Eight implanted tumors showed arterial enhancement on attenuation measurements among the nine tumors for which unenhanced scans were available. Most of the implanted tumors showed persistent enhancement on equilibrium phase images. On visual estimation, three enhancing patterns of implanted tumors were detected: isodense to the intercostal muscles on all three phases in three nodules, hyperdense on all three phases in seven, and hyperdense on arterial phase and isodense on equilibrium phase in seven. These findings are somewhat similar to the results of our previous study [13]. However, these results are quite different from the typical enhancing patterns of HCCs in the liver especially during the equilibrium phase when HCCs usually appear hypodense. The difference in enhancement pattern between implanted tumors and HCCs in the liver during the equilibrium phase is probably because the liver and the surrounding tissue where the implanted tumor is located have different blood supplies. The liver parenchyma is supplied by both the hepatic arterial and the portal venous systems, whereas the surrounding tissue is supplied only by the systemic arteries.
Although the CT techniques were diverse, the injection methods of contrast material, such as timing, rate, and the use of a power injector, were fairly constant, which gives us confidence about the CT features noted in our study. Therefore, if we observe the characteristic morphology and arrangement of tumor through the previously used needle tract in the abdominal or chest wall in the absence of washout on equilibrium phase, which is characteristic of intrahepatic HCC, the diagnosis of needle tract implantation of HCC can be given confidently.
In conclusion, sonographically guided percutaneous biopsy of HCC may be associated with needle tract implantation tumors; although rare, these tumors occur mainly in patients who undergo biopsy of HCCs with end-cutting needles. The CT features of extrahepatic implantation tumors of HCC are similar to those reported previously. Their doubling times are similar to those of the HCCs in the liver.
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