Subsegmental Transcatheter Arterial Embolization for Hepatocellular Carcinoma in the Caudate Lobe

Subsegmental Transcatheter Arterial Embolization for Hepatocellular Carcinoma in the Caudate ~ o b e ' Noboru Terayama, MD Shiro Miyayama, MD Hiroki Tatsu, MD Tatsuya Yamamoto, MD Daishu Toya, MD Nobuyoshi Tanaka, MD Takeshi Mitsui, MD Shoji Miura, MD Masakiyo Fujisawa, MD Koichi Kifune, MD Osamu Matsui, MD Tsutomu Takashima, MD

Index terms: Embolization Liver neeplasms, chemotherapeutic infusion

JVIR 1998;9:501-508 Abbreviations: DSA = digital subtraction angiOgraphy, HCC = hepatocellular carcinoma, PEI = percutaneous ethanol injection, TAE = transcatheter arterial embolization, TAI = transcatheter arterial infusion therapy

From the Departments of Radiology (N. Terayama., S.M., H.T., T.Y.), Internal Medicine (D.T., N. Tanaka), and Surgery (T,M,, S,M,, M,F.), Fukuiken Saiseikai Hospital, Fukui, 918-8503 and the Department of Radiology (N. Terayama, H.T., K.K., O.M., T.T.1, Kanazawa University School of Medicine, Kanazawa 920-8640 Japan. Received August 20, 1997; revision requested October 9; revision received November 25; accepted NO"ember 27. Address correspondence to N. Terayama.

o SCVIR,

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PURPOSE: To clarify the effectiveness of transcatheter arterial embolization (TAE) for hepatocellular carcinoma (HCC) in the caudate lobe of the liver. MATERIALS AND METHODS: Thirteen patients with HCC in the caudate lobe underwent TAE. TAE was performed by injection of the mixture of anticancer drugs (mitomycin C and doxorubicin or epirubicin) and iodized oil, followed by gelatin sponge particles. Arterial anatomy of the caudate branch, local recurrence rate, and survival rate were evaluated. RESULTS: From 31 TAEs for the caudate lobe, 22 subsegmental TAEs were successfully performed (71%).Local recurrence in the caudate lobe was seen in 10 patients (77%).Subsegmental TAE for the caudate lobe was repeated one to five times. Cumulative local recurrence rates were 33% and 75%within 3 and 6 months, respectively. Survival rates after first TAE for HCC in the caudate lobe were 89% and 74%for 1 and 3 years, respectively. CONCLUSION: Local recurrence rate after subsegmental TAE for HCC in the caudate lobe was high. However, repeated subsegmental TAE possibly improves the prognosis of HCC in the caudate lobe.

THE prognosis of patients with hepatocellular carcinoma (HCC) has been improved with advances in several therapeutic options, such as transcatheter arterial embolization (TAE), and percutaneous ethanol injection (PEI), in addition to surgical resection (1).However, the treatment for HCC arising in the caudate lobe is often difficult because the caudate lobe is anatomically located between the right and left lobes of the liver and near the hepatis and inferior vena cava (2-5). Moreover, HCC in the caudate lobe frequently form tumor thrombi both in the portal vein and inferior vena cava (6). Surgical resection of the caudate lobe has a high mortality rate, and the recurrence rate of HCC in the caudate lobe after surgical resection is

higher than that of HCC arising in other lobes (7-9). PEI for HCC in the caudate lobe may not always be safe because the tumor sometimes exists near the large vessels. It is also difficult to achieve complete necrosis of HCC in the caudate lobe with conventional TAE, which is performed from the right or left hepatic artery because the tumor sometimes has multiple feeding arteries deriving from the proximal portion of the right andlor left hepatic arteries (10). Takayasu et al described four of five patients with HCC in the caudate lobe who undement transcatheter arterial infusion therapy (TAI) or TAE and died a mean period of 5.5 months after the initial diagnosis (6). Recently, with advances in microcatheters and digital subtraction

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Table 1 Size and Location of Tumor in 13 Patients with HCC in the Caudate Lobe

Patient

Age (y)

1 2 3 4 5 6 7 8 9 10 11 12 13

58 67 67 54 64 83 55 73 55 77 59 76 72

HCC in S 1

Main Tumor

Sex

Segment of Primary HCC

Location

Size (cm)

Segment

F F F F F F F F F M M F M

S4 S1,5 S2-4 S1,4,8 S1 S1,2/3 S1 S8 S1 S1,2,4,6,7 S1,3 S1,8 S1,8

PCISP CP SP SP PC PC CP SP SP SP PC PC CP

1.510.5 3 1.2 2 3 2 3 4 3 0.5 1 4 3.5

S4 S1 S2 S4 S1 S3 S1 S518 S1 S7 S1 S8 S1

Size (cm)

Other Treatment

3 2 2.5 3

PEI for S3

5

S8 P.O., PEI for S518

3 8

Note.-S1 = caudate lobe; S1-8 = liver segment according to Couinaud's classification; PC = paracaval position; S P Spiegel lobe; CP = caudate process; PEI = percutaneous ethanol injection; P.O. = postoperation.

angiography (DSA) systems, it is possible to insert the microcatheter intentionally into more distal branches of the subsegmental artery of the liver. Therefore, embolization of the tumor-bearing subsegment of the liver (subsegmental TAE) is possible and good results of subsegmental TAE for small HCC have been reported (11,121. We applied subsegmental TAE for HCC arising in the caudate lobe in 13 patients. In the present study, subsegmental TAE indicated that from the caudate branch or more distal branch. TAE for the caudate lobe from the segmental artery involving the other subsegment was defined as segmental TAE. We analyzed the feeding arteries of tumors, the success rate of superselective catheterization into the feeders, the local recurrence rate of HCC after subsegmental TAE, and the survival rate after initial subsegmental TAE for HCC in the caudate lobe.

MATERIALS AND METHODS Between April 1993 and March 1997, 578 TAE or TAI treatments were performed for 291 patients with HCC in our hospital. During the same period, 13 patients with HCC in the caudate lobe underwent TAE treatment (Table 1).The

group of 13 patients consisted of three men and 10 women who ranged in age from 54 to 83 years (mean, 66 years). All 13 patients were liver cirrhosis related with viral hepatitis C. Seven patients were classified as Child class A, three as Child class B, and three as Child class C. The diagnosis of HCC was made by nodular stain on DSA and nodular perfusion defect on computed tomography (CT) during arterial portography, which were simultaneously performed. In 10 of 13 patients, HCC originated in the caudate lobe. Among them, seven patients had HCCs in the other segments and three patients had solitary HCCs in the caudate lobe. TAE for HCCs in the other segments was also performed. In the remaining three patients, HCC occurred in the caudate lobe during follow-up after treatment for HCC in the other segments. In two of three patients, recurrent HCC was seen in the other segments when TAE for HCC in the caudate lobe was performed. Two patients underwent PEI for HCC in the other segment after TAE for the caudate lobe. The size of HCC in the caudate lobe ranged from 0.5 to 4.0 cm. The location of HCC in the caudate lobe was determined by CT according to Kumon's criteria, in-

=

cluding the Spiegel lobe, the caudate process, and the paracaval portion (4,5). HCC was detected in the Spiegel lobe in five patients, in the paracaval portion in four patients, in the caudate process in three patients, and in both the Spiegel lobe and the paracaval portion in one ~ a t i e n tThe . total number of TAE procedures, including that for other segments, ranged from one to 11 times (mean, four times). No patients underwent other treatment for HCC in the caudate lobe except TAE or TAI therapy. The feeding arteries of HCCs in the caudate lobe are listed in Table 2. There were three feeding arteries in one patient (two deriving from the right hepatic artery and one from the posterior branch of the right hepatic artery), two feeding arteries in three patients (deriving from the anterior branch of the right hepatic artery and the right inferior phrenic artery, the right hepatic artery and the anterior superior branch, left and right hepatic arteries in one patient each), and one feeding artery in nine patients (deriving from the left hepatic artery in five patients, the right hepatic arteryin two patients, the proper hepatic artery in one patient, and the posterior branch in

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Table 2 Results of TAE for HCC in the Caudate Lobe TAE for HCC in Feeding Artery S1 (No. of instances) of HCC in S1 Total Is Deriving From Instances SubSegmental or Patient (on 1st TAE for S1) of TAE* segmental larger area TAI 1 2 3 4 5 6 7 8 9 10 11 12 13

IPA, ANT LHA PHA LHA RHAx2, POST LHA RHA, A8 LHA§ LHA RHA RHA LHA, RJw POST

11 2 5 7 5 2 3 1 5 2 1 7 1

1(2)$ 1 1 1 3 2 2 1 3 1 1 5 0

1 1

2 1

1 1

Status (mo)t/Cause of Death 19.5 5.1 20.6 24.3 14.5 12.5 25.7 1.2 29.9 4.5 5 39.3 5

Deadtumor progression Deadtumor progression Alive, recurrence (+) Alive, recurrence in other segment Alive, recurrence (+) Alive, recurrence (+) Deadhepatic failure, recurrence (-1 Alive, recurrence (-1 Alive, recurrence (-1 Deadlrupture of esophageal varices, recurrence (+) Alive, recurrence (-1 Deadtumor progression Deadthepatic failure, recurrence (+)

Note.-S1 = caudate lobe; IPA = inferior phrenic artery; ANT = anterior branch of right hepatic artery; LHA = left hepatic artery; PHA = proper hepatic artery; POST = posterior branch of right hepatic artery; A8 = anterior superior branch of right hepatic artery; 5 = caudate branch derived from the common branch with accessory left gastric artery; I/ = caudate branch derived from the common branch with cystic artery. " Including TAI. t Months from first TAE for HCC in S1. $ There were two HCCS in the caudate lobe, TAE once for one HCC and two times for the other.

one patient). The location of branching is shown in Figure 1. TAE procedures were as follows: a 4-F or 5-F catheter was inserted into the celiac artery or common hepatic artery. After observation of the feeding arteries on DSA images, a microcatheter (Microferret; Cook, Bloomington, IN or Tracker-18; Target Therapeutics, Fremont, CA) was inserted into the feeding artery by means of a coaxial method with use of a 0.016-inch guide wire (Radifocus GT wire; Terumo, Tokyo, Japan). Lidocaine (0.5-1.0 mL) was then injected into the feeding artery to prevent pain and vasospasm. The mixture of anticancer drugs and iodized oil (Lipiodol; Andre Guerbet, Aulnaysous-Bois, France) was then injected and the feeding artery was embolized with gelatin sponge particles (Gelfoam; Upjohn, Kalamazoo, MI). The mixture of anticancer drugs contained 2-6 mg of mitomycin C, 10-30 mg of doxorubicin or epirubicin, 1-3 mL of iodized oil, and 0.5-1.0 mL of iopamidol. Anticancer drugs and iodized oil were mixed by repeated pumping approx-

imately 10 times through a threeway stopcock. The gelatin sponge was cut into 1-mm cubes and the particles were then immersed in iopamidol. Gelatin sponge particles were injected until the feeding artery was completely obliterated. TAI was performed in the same method except embolization was performed with gelatin sponge particles. One patient had two HCCs in the caudate lobe supplied by the right inferior phrenic artery and the anterior branch of the right hepatic artery separately (patient 1, Fig 2). In this case, two selective TAE procedures were successfully performed for the HCC supplied by the inferior phrenic artery. Although four subsegmental TAEs were attempted for the other HCC, it was successful only once. A microcatheter with its tip bent into a J shape was often used to enable insertion into the caudate branches, especially those deriving from the proper hepatic artery or proximal portion of the right or left hepatic arteries. In one patient in whom the caudate

branch, deriving from the left hepatic artery accompanied by the accessory left gastric artery (patient 8, Fig 3), was too small in caliber to insert a microcatheter, the accessory left gastric artery was first blocked with use of a microcoil and n-butyl cyanoacrylate. The mixture of anticancer drugs was then injected and embolized with gelatin sponge particles. In serial TAE treatment, changes of feeding arteries were observed in two patients. A newly formed, complicated intrahepatic anastomosing branch supplied HCC in the caudate lobe in one patient. The inferior phrenic artery began to supply the HCC in the caudate lobe in the other patient. Local recurrence was judged by the irregular-shaped defect of accumulation of iodized oil in the lesion and early contrast material enhancement on dynamic CT or tumor stain on DSA. One of these imaging methods was performed within 3-4 months after TAE for HCC in the caudate lobe. Cumulative local recurrence rate and survival rate af-

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I P A 1 (PC

LHA 6 (CP 1, PC 2, SP

(CP 1, PC 4, SP1) Figure 1. Vascular anatomy of the caudate branch. Site of branching and the number of the feeding arteries of HCC in the caudate lobe (ZPA = inferior phrenic artery; LHA = left hepatic artery; PHA = proper hepatic artery; RHA = right hepatic artery; POST = posterior branch of the right hepatic artery; ANT = anterior branch of the right hepatic artery; A1-8 = according to the Couinaud classification; CP = caudate process; PC = paracaval portion; S P = Spiegel lobe location of HCC in the caudate lobe).

ter the first TAE for HCC in the caudate lobe were calculated with use of the Kaplan-Meier life-table analysis.

I RESULTS Local Control Effects of Subsegmental TAE From 31 TAEs for HCC in the caudate lobe, subsegmental TAE for HCC in the caudate lobe was successfully performed 22 times (71%, Figs 2-5). This meant success of insertion of a microcatheter into the caudate branch, administration of the drug, and embolization of the caudate branch; in addition, confirmation of disappearance of tumor stain on DSA after

TAE. The reasons for the technically unsuccessful cases were failure of identification of the feeding artery, of insertion of a guide wire, and of insertion of a microcatheter. Accumulation of iodized oil throughout the tumor was seen on follow-up CT 1 week after TAE in the same number of instances. Subsegmental TAE for HCC in the caudate lobe was performed in 12 of 13 patients (92%, Table 2). There were no major complications, but mild abdominal pain and low-grade fever lasted for 1 week. Recurrence of HCC in the caudate lobe was seen in 10 patients (77%). TAE for recurrent HCC in the caudate lobe was repeated. The number of subsegmental TAEs performed for HCC in

the caudate lobe ranged from one to five instances.

Long-term Outcomes Cumulative local recurrence rates were 33% and 75% within 3 and 6 months, respectively (Fig 6). Three patients died of tumor progression, including that in the caudate lobe at 39.3, 19.5 and 5.1 months after first TAE for HCC in the caudate lobe. Two patients showed recurrence in the caudate lobe and died of hepatic failure or rupture of esophageal varices at 5 and 4.5 months after TAE. One patient without recurrence died of hepatic failure 25.7 months after TAE. Survival rates after the first TAE for HCC in the caudate lobe were 89% and 74% for 1and 3 years, respectively (Fig 7).

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a.

b.

c.

Figure 2. Patient 1. (a) HCC (arrow) in the caudate lobe is supplied by the right inferior phrenic artery. The lower stain represents the right adrenal gland. (b)Celiac angiography 14 months after initial TAE for the caudate lobe shows tumor stain of the HCC (arrowheads) in the caudate lobe. The caudate branch (thin arrows) derives from the anterior branch of the right hepatic artery. One of the HCCs in the other segments is also seen (thick arrow). ( c ) A microcatheter is inserted into the caudate branch deriving from the anterior branch of the right hepatic artery. The whole of the caudate lobe is involved by HCC. TAE for the other segments has been performed already. (d) Plain CT shows accumulation of Lipiodol in the HCC in the caudate lobe (asterisk). Lipiodol in HCC in the other segments are also seen. d.

Figure 3. Patient 8. The caudate branch (thin arrow) derives from the left hepatic artery accompanied by the accessory left gastric artery (thick arrow). TAE for the caudate lobe was performed after embolization of the accessory left gastric artery using a microcoil and n-butyl cyanoacrylate. The left stain (arrowheads) represents HCC in the caudate lobe and the right stain represents the fornix of the stomach.

DISCUSSION Liver segment, as defined by Healey and Schroy or Couinaud, is generally used for the description of segmental anatomy (2,3). However, neither clearly define the border of the caudate lobe. Kumon reported detailed anatomy of the caudate branch of the portal vein and bile

duct with use of liver casts of silicone rubber (4). In addition to the Spiegel lobe and the caudate process, the caudate lobe includes the area anterior to the hepatic segment of the inferior vena cava, which was named the paracaval portion of the caudate lobe. The paracaval portion often extends to the surface of the liver just below the diaphragm. The portal branch and bile duct in the Spiegel lobe mainly belong to the left side of the liver, those in the caudate process belong to the right side of the liver, and in most cases, the portal branches of the paracaval portion lead to the first branch of the left portal vein, whereas the biliary ducts lead equally to both lobes. According to the CT analysis (5), the area between the roots of the right hepatic vein and middle hepatic vein belong to the paracaval portion of the caudate lobe, which had been classified as the anterior superior segment in more than 70% of patients. Therefore, we regarded that the paracaval portion belonged to the caudate lobe and patients with HCC in the paracaval portion were included in the present study. Regarding the artery of the cau-

date lobe, Michels stated that the caudate branch derived from the right hepatic artery in 60% of patients, both the right and the left hepatic artery in 14%, the middle hepatic artery in 6%, the left or the right and middle hepatic artery in 4%, and the common or proper hepatic artery in 8% (13). In a study by Miyayama et a1 (101, the number of caudate branches of the hepatic artery was one in 70.8% of patients and two in 14.2% of patients on angiography. The caudate branch derived from the proximal right hepatic artery in 50% of patients and from the left hepatic artery in 7.5% of patients (10). The left lobe of the liver is short in depth, so the caudate branch sometimes cannot be confirmed even on stereo angiography. Consequently, the ratio of the caudate branch from the left hepatic artery might be underestimated. When HCC occurs in the caudate lobe, dilatation of the caudate branch of the hepatic artery may occur, making it easier to identify the caudate branch. Similar to the caudate branch of the portal vein, HCC in the Spiegel lobe tends to be supplied by the left side. However, those in the paracaval portion

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Figure 4. Patient 4. (a) Celiac angiography shows HCC (arrow) in the caudate lobe. The caudate branch (arrowheads) derives from the left hepatic artery. (b)A microcatheter is inserted into the caudate branch. ( c ) Plain CT 1week after TAE shows accumulation of Lipiodol in the HCC (asterisk) in the Spiegel lobe. Overflowed Lipiodol is scattered in the nontumorous liver.

and the caudate process tend to be supplied by the right side. However, HCC in the edge of the Spiegel lobe was supplied by the branch belonging to the anterior branch of the right hepatic artery in one patient. The inferior phrenic artery possibly supplied HCC in the caudate lobe. As such, it is necessary to assess the feeding artery carefully. Yamada et a1 reported in their large series of more than 1,000 patients with HCC who were treated with conventional TAE with gelatin sponge particles and anticancer drugs, that I-, 2-, 3-, 4-, and 5-year survival rates were 51%, 28%, 13%, 8%, and 6%, respectively (14). Ohishi et a1 reported a 4-year survival rate of 20.4% after conventional TAE with iodized oil for more than 500 patients (15). Kawasaki et a1 reported that the 4-year survival rate of patients with HCC who were treated with subsegmentectomy was 49% (16). According to the report from the Liver Cancer Study Group of Japan, 1-6-year survival rates of hepatectomy were 84.7%, 74.3%, 65.0%, 55.1%, 46.3%, and 41.8%, respectively (1). In the same reports, 1-4-year survival rates of PEI were 86.4%, 67.0%, 51.5%, and 37.1%, and 1-5-year and 10-year survival rates of TAE were 54.4%, 31.8%, 19.5%, 12.5%, 9.2%, and 2.3%, respectively. Segmental or subsegmental TAE was devised to obtain long-term control of HCC and to prevent loss of liver function (11,12). Improvement of microcatheter and guide-

Figure 5. Patient 2. (a) A microcatheter is inserted into the caudate branch deriving from the left hepatic artery. The whole of the stain represents HCC in the caudate lobe. (b) Lipiodol is accumulated in HCC in the caudate lobe.

wire systems has enabled easier access to distal branches of the hepatic artery, such as the segmental or subsegmental branches. The three-year survival rate of segmental TAE with iodized oil for HCCs less than 5 cm was 55% (11). One and 4-year survival rates of the patients treated with subsegmental TAE were 100% and 67%, respectively (12). One to 5-year survival rates of hepatectomy for HCC less than 5 cm were 85.8%, 75.3%, 65.4%, 54.8%, and 45.8% (1). The effect of subsegmental TAE for small HCCs is comparable to that of surgical resection or PEI (12). Surgical resection of HCC in the caudate lobe has a higher surgical risk and higher rate of early recurrence (7-9). Hepatic reserve restricts the indication of surgical resection. Shimada et al reported that six of eight patients with 6 months or longer follow-up had recurrences

and two of six patients died (7). Nagasue et a1 reported that a 5-year survival rate after the resection of the caudate lobe was 31.3%, and it was significantly better in patients with primary HCC than in those with recurrent tumors (49.2% compared with none) because of frequent recurrence in the latter group (9). Recently, microwave coagulation therapy and CT-guided PEI for HCC in the caudate lobe were reported (17,18). However, because of its anatomical location close to the porta hepatis and large vessels, these procedures are not always performed safely and easily. HCC in the caudate lobe frequently formed tumor thrombi both in the portal vein and inferior vena cava, resulting in both intrahepatic and extrahepatic metastases (6). In the present study, follow-up CT 3 months after subsegmental TAE revealed recurrent HCC in the cau-

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Survival rate (%)

Local recurrence rate (%)

10

20

0 1

0

(Months)

I

I

I

10

7.

20 (Months)

30

II

40

Figures 6, 7. (6) Cumulative local recurrence rate after first TAE for the HCC in the caudate lobe. Recurrence rates are 33.3% and 75.0%within 3 and 6 months, respectively. Broken lines indicate 95% confidence limits. (7) Survival rate of 13 pa-

tients who underwent TAE for HCC in the caudate lobe. One-year and 3-year survival rates after first TAE for the caudate lobe are 88.9% and 74.1%,respectively. Broken line indicates 95% confidence limits. date lobe forming tumor thrombus in the portal vein, and the patient died approximately 5 months after the first TAE. Takayasu et a1 reported that four of five patients with HCC in the caudate lobe who underwent TAI or TAE died a mean period of 5.5 months after the initial diagnosis (6). In the present study, cumulative local recurrence rates of TAE for the caudate lobe were much higher (33.3% and 75.0% within 3 and 6 months) than those of subsegmental TAE for HCC in the other segments (18% and 30% within 1 and 2 years) (12). However, survival rates of subsegmental TAE for HCC in the caudate lobe (88.9% and 74.1% for l and 3 years, respectively) were comparable with those of surgical resection of the caudate lobe (31.3% for 5 years) (9) or other segments (1,16). It was also much better than that of conventional TAE for HCC in the caudate lobe (6). The local recurrence rate of TAE for the caudate lobe was high; however, repetitive subsegmental TAE can possibly improve the prognosis of HCC in the caudate lobe. During the TAE procedure, iodized oil injected into a hepatic artery is occasionally seen in the portal veins, resulting in embolization of both the hepatic artery and portal vein (19). I t is known that a relatively large amount of iodized oil

for the limited liver area bearing HCC induced parenchymal atrophy (20). However, in the present study, there were no cases showing parenchymal atrophy of the caudate lobe as is sometimes seen after subsegmental TAE for HCC in other segments. This indicated that complete blockage of the blood flow was not achieved. We think that complete necrosis of HCC in the caudate lobe after subsegmental TAE seldom occurs and the following points are possibly responsible. HCC in the caudate lobe is potentially supplied by multiple feeding arteries, and 30% of HCC cases had multifeeder a t the time of diagnosis in our study. The caudate branches of the hepatic artery are derived from the proximal portion of the right hepatic artery andlor left hepatic artery, so it is frequently difficult to not only confirm but also insert the microcatheter into the feeding artery. Furthermore, complete blockage of the tumor vessels with embolic materials may be impossible when the tumor is supplied by multiple feeders. When the embolic materials were injected from one of the feeding arteries, the collateral blood flow through the other feeding arteries reversed the blood flow of the embolized artery and pushed back the embolic materials. In conclusion, cumulative local recurrence rate after subsegmental

TAE for HCC in the caudate lobe was very high compared with recurrence rate after subsegmental TAE for HCC in the other segments. However, survival rates were comparable with those of surgical resection. Repetitive subsegmental TAE possibly improves the prognosis of HCC in the caudate lobe. References

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