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Comparison of CT Findings with Resected Specimens After Chemoembolization with Iodized Oil for Hepatocellular Carcinoma

¹ Department of Diagnostic Radiology, National Cancer Center Hospital, 5-1-1, Tsukiji, Chuo-ku, Tokyo 114-0045, Japan.
² First Department of Surgery, Kyoto University, 54, Kawara-cho, Seigoin, Sakyo-ku, Kyoto 606-8507, Japan.
³ Department of Radiology, Nara Prefectural Medical College, 840, Shijo-cho, Kashihara, Nara 634-8522, Japan.
⁴ First Department of Medicine, Chiba School of Medicine, 1-8-1, Inohana, Chuo-ku, Chiba 260-8766, Japan.
⁵ Department of Surgery, National Cancer Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa, Chiba 277-0882, Japan.
⁶ Department of Surgery, Tokyo Women's Medical College, 8-1, Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan.
⁷ Department of Radiology, Wakayama Prefectural Medical College, 811-1, Kimidera, Wakayama 641-8509, Japan.
⁸ First Department of Surgery, Hyogo School of Medicine, 1-1, Bukogawa-cho, Nishimiya, Hyogo 663-8501, Japan.
⁹ Department of Surgery, Chiba-nishi Hospital, 107-1, Kanegasaku, Matsudo, Chiba 270-2251, Japan.

Received May 18, 1999; accepted after revision January 4, 2000.

 
Supported in part by the Liver Cancer Study Group of Japan.

Address correspondence to K. Takayasu.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. We assessed the role of dynamic CT in the evaluation of the efficacy of transarterial chemoembolization with iodized oil for hepatocellular carcinoma.

MATERIALS AND METHODS. We examined 41 hepatocellular carcinoma lesions (mean diameter, 5.0 cm) in 40 patients (mean age, 60.6 years) who underwent transarterial injection of iodized oil alone (n = 3) or emulsion of iodized oil and doxorubicin hydrochloride (n = 10) followed by gelatin sponge particles (n = 27) and subsequent hepatectomy. On dynamic CT performed within 3 weeks before oily transarterial chemoembolization and within 4 weeks before surgery, we calculated the rate of necrosis on the basis of the assumption that the portion that retained iodized oil represented necrosis. We also calculated the reduction rate of the tumor. CT findings were compared with pathologic findings of resected specimens.

RESULTS. Pathologic specimens and the necrosis rate measured on CT showed a good correlation (r = 0.83) when the portion of tumor that retained iodized oil was considered necrosis. No correlation existed if the portion that retained iodized oil was considered viable. We noted no significant correlation (r = 0.38) between the reduction rate of the tumor and necrosis rate. Also, we noted no correlation (r = 0.52) between the interval between transarterial oily chemoembolization and surgery and the reduction rate of the tumor.

CONCLUSION. CT is suitable for the evaluation of the efficacy of oily chemoembolization for hepatocellular carcinoma on the basis of the assumption that the portion of tumor that retains iodized oil is necrotic. The rate of tumor size reduction measured on CT did not correlate with the therapeutic effect of chemoembolization.

Introduction

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Transarterial chemoembolization with iodized oil (Lipiodol UltraFluid; Andre Guerbet, Aulnay-sous-Bois, France) is now performed worldwide for nonoperable and recurrent hepatocellular carcinoma [1,2,3,4,5,6,7]. To evaluate its efficacy, dynamic contrast-enhanced CT is generally performed. Before iodized oil was clinically introduced to transarterial chemoembolization therapy as a vehicle to transport anticancer drugs to sites of hepatocellular carcinoma, dynamic CT was the most reliable tool for the assessment of the efficacy of transarterial chemoembolization [8]. On CT, necrosis appears unenhanced, and viable tumors appear enhanced. However, with the introduction of iodized oil, the evaluation of transarterial oily chemoembolization on dynamic CT became difficult because lesions retain iodized oil, which has a high attenuation on CT. Some lesions were histopathologically verified to be viable (Fig. 1A,1B,1C), even though a relatively good retention of iodized oil was recognized on unenhanced CT; however, other lesions revealed opposite features. Only a few articles describe the use of CT to evaluate the efficacy of transarterial oily chemoembolization [9,10,11,12]. To our knowledge, no study exists that compares CT findings with resected specimens with emphasis on the assessment of retained iodized oil in the tumor. Specifically, no article addresses whether the portion of tumor that retains iodized oil is necrotic or viable cancer tissue.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —47-year-old man with solitary hepatocellular carcinoma who underwent injection of emulsion of 5 mL of iodized oil and 20 mg of doxorubicin hydrochloride in proper hepatic artery. Unenhanced CT scan reveals retention of iodized oil in lesion (arrows).

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —47-year-old man with solitary hepatocellular carcinoma who underwent injection of emulsion of 5 mL of iodized oil and 20 mg of doxorubicin hydrochloride in proper hepatic artery. Early enhanced CT scan shows slight enhancement of peripheral (arrows) and central portions of lesion suggestive of viable cancer tissue.

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —47-year-old man with solitary hepatocellular carcinoma who underwent injection of emulsion of 5 mL of iodized oil and 20 mg of doxorubicin hydrochloride in proper hepatic artery. Cut surface of resected specimen obtained 36 days after A shows histopathologically verified fully viable tumor.

The criteria proposed by the World Health Organization have generally been used for evaluating the effect of chemotherapy on cancer [13]. Namely, the rate of reduction or increase of tumor size was calculated by physical examination or imaging in comparison with tumor size before and after therapy. However, these criteria cannot be applied to the evaluation of transarterial chemoembolization therapy because tumor reduction is seldom recognized before 4 weeks after treatment, even though the tumor may be completely necrotic (Fig. 2A,2B,2C).

View larger version (74K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —66-year-old woman with small hepatocellular carcinoma who underwent injection of emulsion of 7 mL of iodized oil and 25 mg of doxorubicin hydrochloride followed by Gelfoam particles (Upjohn, Kalamazoo, Ml) in right hepatic artery. Dynamic CT scan reveals enhancing tumor measuring 2.5 x 2.5 cm in diameter in segment VIII [26].

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —66-year-old woman with small hepatocellular carcinoma who underwent injection of emulsion of 7 mL of iodized oil and 25 mg of doxorubicin hydrochloride followed by Gelfoam particles (Upjohn, Kalamazoo, Ml) in right hepatic artery. Dynamic CT scan obtained 117 days after A shows dense deposition of iodized oil in tumor that measures 2.0 x 2.0 cm. Enhancement of tumor was not seen, suggesting complete necrosis. Reduction rate was 36%.

View larger version (111K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —66-year-old woman with small hepatocellular carcinoma who underwent injection of emulsion of 7 mL of iodized oil and 25 mg of doxorubicin hydrochloride followed by Gelfoam particles (Upjohn, Kalamazoo, Ml) in right hepatic artery. Cut surface of specimen resected 23 days after B shows completely necrotic tissue with thick fibrous capsule.

Therefore, we retrospectively compared CT findings with resected hepatocellular carcinoma specimens that were treated with transarterial oily chemoembolization. We also studied which factor reflects the real efficacy of transarterial oily chemoembolization, the necrosis rate (percentage) or the reduction rate of the tumor, using three different therapeutic agents that were not randomly assigned.

Materials and Methods

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Between September 1990 and August 1996, 151 patients with hepatocellular carcinoma who underwent transarterial oily chemoembolization followed by hepatectomy at nine institutions were examined to determine the efficacy of transarterial oily chemoembolization. Of these patients, we examined 40 with 41 hepatocellular carcinoma lesions. Patients who participated in our investigation satisfied three criteria. First, the patients were required to have undergone dynamic CT, including unenhanced CT, within 3 weeks of undergoing transarterial oily chemoembolization (CT performed before transarterial chemoembolization) (Fig. 3A) and within 4 weeks of undergoing surgery (CT performed after transarterial chemoembolization) (Fig. 3B); second, all patients had lesions that were measurable on CT; and third, the patients had resected specimens that were cut in slices 10 mm or thinner, which corresponded to CT slices (Fig. 3C). In this paper, the term "transarterial oily chemoembolization" is used as a general term including iodized oil alone and emuision of iodized oil and anticancer agent with or without gelatin sponge particles (Gelfoam; Upjohn, Kalamazoo, MI). Thirtynine patients had one lesion each, and one patient had two lesions. We examined 33 men and seven women (age range, 40-81 years; mean age, 60.6 years). The mean diameter of hepatocellular carcinomas was 5.0 cm (range, 1.8-14.5 cm). The mean intervals between CT performed before transarterial chemoembolization and transarterial oily chemoembolization, between CT performed after transarterial chemoembolization and surgery, and between transarterial oily chemoembolization and surgery were 6.9 days (range, 2-21 days), 11.7 days (range, 1-30 days), and 57.6 days (range, 19-158 days), respectively. Noncancerous tissue of the liver was shown on histopathology to be normal in one patient, chronic hepatitis in seven, and cirrhosis in 32.

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —45-year-old man with incidentally found tumor who underwent injection of emulsion of 5 mL of iodized oil and 20 mg of doxorubicin hydrochloride followed by Gelfoam particles (Upjohn, Kalamazoo, Ml) in proper hepatic artery. Dynamic CT scan obtained during portal dominant arterial phase reveals large encapsulated hepatocellular carcinoma measuring 10.7 x 8.1 cm homogeneously enhanced except for central unenhanced area (necrosis). Oily chemoembolization was performed 6 days later.

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —45-year-old man with incidentally found tumor who underwent injection of emulsion of 5 mL of iodized oil and 20 mg of doxorubicin hydrochloride followed by Gelfoam particles (Upjohn, Kalamazoo, Ml) in proper hepatic artery. Dynamic CT scan obtained during early phase (58 days after A) reveals scattered depositions of iodized oil and small enhancing area (arrow) measuring 8.7 x 7.4 cm. Necrosis rate in tumor was 75%. Enhanced dorsal portion changed to low attenuation in late phase (not shown). Reduction rate was 25.7%.

View larger version (144K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —45-year-old man with incidentally found tumor who underwent injection of emulsion of 5 mL of iodized oil and 20 mg of doxorubicin hydrochloride followed by Gelfoam particles (Upjohn, Kalamazoo, Ml) in proper hepatic artery. Cut surface of specimen resected 15 days after B shows coagulative necrosis of entire tumor except for viable cancer tissue with hemorrhage in dorsal portion (arrows) that corresponds to contrast-enhanced area in B.

Unenhanced CT followed by dynamic incremental CT (TCT 900S, Toshiba, Tokyo, Japan; HiLight Advantage, General Electric Medical Systems, Milwaukee, WI) or helical CT (X-vigor, Toshiba; HiSpeed Advantage, General Electric Medical Systems; Somatom Plus 4, Siemens, Erlangen, Germany) was performed with a 7- to 10-mm slice thickness at a speed of 7-10 mm/sec with table increments. Dynamic CT started 35-45 sec after the IV injection of 100-120 mL of contrast material (65% meglumine diatrizoate, Schering, Kenilworth, NJ; 300 mg I/mL iopamidol, Schering, Tokyo, Japan) at a speed of 2-3 mL/sec (early phase contrast-enhanced CT) or 4-5 min later for late phase contrast-enhanced CT.

For embolization, 5 mL of iodized oil was injected into three hepatocellular carcinomas in three patients, 5-7 mL of iodized oil mixed with 20-30 mg of doxorubicin hydrochloride dissolved in ionized or deionized contrast medium (half the volume of iodized oil) was injected into 10 hepatocellular carcinomas in 10 patients, and subsequently gelatin sponge particles were injected into 28 hepatocellular carcinomas in 27 patients. A 5- or 6-French catheter was advanced into the segmental, right, left, or both hepatic arteries depending on the location or size of the lesion, and transarterial oily chemoembolization was performed. For one patient with two hepatocellular carcinomas localized in the right anterior area, transarterial oily chemoembolization was performed in the right hepatic artery. The portal vein was patent in all patients.

To calculate the necrosis rate (percentage) of the lesion on CT, contrast-enhanced, unenhanced, and iodized oil retaining areas were separately measured for density using the slice level with the maximum tumor size (Fig. 3B). The necrosis rate was calculated with the following formula: necrosis rate = (nonenhancing area + area of iodized oil retention) / (total area of tumor) x 100, on the basis of the assumption that the portion of tumor that retained iodized oil was necrotic. But if the portion of tumor that retained iodized oil was presumed to represent viable cancer tissue, the area containing iodized oil would not be added in the numerator.

To calculate the reduction rate of the tumor, the following formula was used: (a x b - a' x b') / (a x b) x 100). The coefficients a and a' are the longest diameter, and b and b' are the perpendicular diameter of the tumor measured on CT before and after transarterial oily chemoembolization. The ring enhancement around the tumor revealed on late phase contrast-enhanced CT was included in the tumor size.

The pathologic necrosis rate, the necrotic area compared with the total area of the lesion, was measured in the cut surface of the largest tumor diameter.

A simple linear regression test was used for statistical analysis, and the regression coefficient was determined.

Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
Relationship of Necrosis Rate Calculated on CT to Histopathologic Necrosis Rate in Resected Specimens
Histopathologically, the mean necrosis rate in the 41 lesions was 67.1% (range, 0-100%). The mean necrosis rate of lesions calculated on dynamic CT was 78.0% (range, 5-100%) if the portion of tumor that retained iodized oil was considered necrotic. A good correlation (r = 0.83) was obtained by comparing the two necrosis rates (Fig. 4). If the portion of the tumor that retained iodized oil was considered viable, the mean necrosis rate calculated on CT was 15.7% (range, 0-80%), and no correlation was noted between CT findings and pathologic measurements (r = -0.04) (Fig. 5).

View larger version (17K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4. —Graph shows relationship between necrosis rate for tumor at maximum tumor size revealed on CT and pathologically proven necrosis rate, based on assumption that portion of tumor that retained iodized oil was necrotic. (r = 0.83)

View larger version (16K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —Graph shows relationship between necrosis rate for tumor at maximum tumor size revealed on CT and pathologically proven necrosis rate, based on assumption that portion of tumor that retained iodized oil was viable cancer tissue. (r=-0.04)

Relationship of Reduction Rate of Tumor to Pathologically Measured Necrosis Rate
To confirm the accuracy of the measurement of tumor size on CT, the product of the longest diameter and the perpendicular diameter of the tumor measured on CT before surgery was compared with the product of the same dimensions on the resected specimen. A good correlation (r = 0.95) was noted. The mean reduction rate of the tumor calculated on CT was 21.2% (range, 18.6 to 67.4%). However, the reduction rate of the tumor and the pathologically measured necrosis rate did not correlate (r = 0.38) (Fig. 6).

View larger version (15K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6. —Graph shows relationship between reduction rate for tumor revealed on CT and pathologically proven necrosis rate for tumor. (r=0.38)

Relationship of the Interval Between Transarterial Oily Chemoembolization and Surgery to the Reduction Rate of Tumor
We noted that the longer the interval between transarterial oily chemoembolization and surgery, the larger the reduction rate of the tumor. However, the measurement was not statistically significant (r = 0.52).

Relationship of the Interval Between CT Performed Before and After Transarterial Chemoembolization to the Degree of Tumor Necrosis
The mean values of the interval between CT performed before and after transarterial chemoembolization and the degree of pathologically proven tumor necrosis were 52.3 ± 31.3 days and 67.9% ± 37.0%, respectively. We found no statistically significant correlation between these two factors (r = 0.0087).

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The major treatment methods for hepatocellular carcinoma—surgery [14], transarterial chemoembolization [4, 5], and percutaneous ethanol injection [15,16,17]—prolong survival. During the past 2 years at our hospital, 672 patients with hepatocellular carcinoma underwent one of the following treatments as an initial therapy: transarterial oily chemoembolization (54.5%), percutaneous ethanol injection (24.2%), surgery (20.6%), or other therapy (0.7%) (unpublished data). Even though chemoembolization was the most frequent therapy, the pathologic study of resected specimens after transarterial oily chemoembolization indicated the presence of residual cancer tissue around the lesion [9], suggesting a high rate of local recurrence. Combination therapy of transarterial oily chemoembolization and percutaneous ethanol injection [18] or proton radiation [19] has also been performed, providing longer survival than transarterial oily chemoembolization alone. Therefore, the evaluation of the efficacy of transarterial oily chemoembolization for hepatocellular carcinoma is indispensable in determining subsequent treatment.

The evaluation of treatment efficacy for cancer has been performed on the basis of reduction rates proposed by the World Health Organization [13]. The complete disappearance of tumor is designated as complete response, a 50% or more decrease in tumor as partial response, a less than 50% decrease or 25% increase in tumor as no change, and a 25% or more increase as progressive disease. This criterion has several advantages; the tumor reduction rate is easily measurable on sonography, unenhanced CT, or both, which are low-cost procedures that are available worldwide even in developing countries. However, this criterion also has some disadvantages. Tumor size has to be evaluated by two time-spaced observations, which means that a long duration is needed to confirm efficacy because some lesions may show complete response 1 year after transarterial oily chemoembolization, and a large discrepancy is commonly recognized between the tumor reduction rate on imaging and the degree of histopathologic necrosis [20].

Our findings show no correlation between tumor size reduction and the histopathologic necrosis rate in resected specimens (Fig. 6). This lack of correlation may be explained if the feeding artery and sinusoid of hepatocellular carcinoma are completely embolized and obstructed when the lesion is totally necrotic. Then the resorption of necrosis is delayed. Similar findings confirmed no correlation between the interval between transarterial oily chemoembolization and surgery and the tumor reduction rate. These changes are at variance with systemic chemotherapy in which complete disappearance of lesions such as liver metastasis is shown on imaging when complete response occurs.

Regarding the relationship of the interval between CT scans performed before and after transarterial chemoembolization to the degree of necrosis, no significant correlation was noted (r = 0.0087). This finding might be explained by noting that the highest degree of necrosis usually occurs immediately after transarterial chemoembolization, and the regrowth of viable cancer cells will occur later if complete necrosis of the tumor was not achieved, which results in a small amount of necrosis during the interval before surgery.

To date, evaluation methods using various imaging techniques have been suggested. Jinno et al. [10] proposed that six patterns of iodized oil deposition in lesions seen on unenhanced CT were useful in evaluating the efficacy of transarterial oily chemoembolization; the complete pattern, in which iodized oil was densely deposited in the whole lesion, showed total necrosis in most lesions, whereas the remaining five patterns showed a wide spectrum of necrosis from 0% to 90%. Choi et al. [11] compared resected specimens with the deposition of iodized oil on unenhanced CT after the injection of an emulsion of iodized oil and doxorubicin. Their findings revealed that complete retention of iodized oil in hepatocellular carcinoma lesions showed a mean necrosis rate of 98% and an incomplete retention, a necrosis rate of 64%. They concluded that incomplete retention of iodized oil corresponds to a wide variation of tumor necrosis, from completely necrotic to viable cancer tissue (Figs. 1A,1B,1C and 3A,3B,3C). Therefore, some investigators emphasize dynamic MR imaging with gadopentetate dimeglumine [21,22,23] or color Doppler sonography [24] as being more accurate than dynamic CT in the evaluation of oily chemoembolization. However, color Doppler sonography may not be as sensitive as dynamic CT in the evaluation of local recurrence [25]. Even though T2-weighted and dynamic MR imaging are useful in the assessment of the viability of the lesion containing iodized oil, they are not helpful in detecting lymph node metastases and small intrahepatic foci. Our findings suggest that the iodized oil deposition in the tumor can be considered necrosis. In the future, a comparative study of imaging and abnormalities using resected specimens may become difficult because nonsurgical interventions such as transarterial chemoembolization and percutaneous ethanol injection are widely used in the treatment of hepatocellular carcinoma and are gradually replacing surgery.

In practice, dynamic CT is preferable in the evaluation of the efficacy of transarterial oily chemoembolization over unenhanced CT because unenhanced CT is incapable of assessing areas without iodized oil deposition [8]. An interval of more than 1 month between transarterial oily chemoinfusion or transarterial chemoembolization and CT is necessary because gradual washout of iodized oil from nonnecrotic portions of tumors and noncancerous hepatic parenchyma with nonspecific deposition will avoid mistakes in evaluating transarterial oily chemoembolization efficacy.

An ideal evaluation of the effect of transarterial oily chemoembolization on imaging may be the analysis of the efficacy on each slice of the whole tumor, even though we used the slice with the maximum tumor size. In the near future, three-dimensional imaging may be necessary to evaluate treatment.

Acknowledgments
 
We thank Fumihiko Wakao, National Cancer Center Hospital; and Kunio Okuda, Chiba University School of Medicine, for his review.

References

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