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Hepatocellular Carcinoma: Involvement of the Internal Mammary Artery¹

¹ From the Department of Radiology, Wakayama Medical University, 811-1, Kimiidera, Wakayama-shi 641-8510, Japan. Received December 3, 1999; revision requested December 28; final revision received June 23, 2000; accepted July 11. Address correspondence to M.N. (e-mail: motoki05@wakayama-med.ac.jp).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To investigate factors related to the development of internal mammary arteries (IMAs) as feeding arteries of hepatocellular carcinomas (HCCs).

MATERIALS AND METHODS: In 30 patients with HCC located in ventral hepatic areas directly beneath the diaphragm, bilateral internal mammary arteriography was performed to explore involvement of the IMA with HCC. The number of previous transcatheter arterial embolizations (TAEs), tumor size, time from initial TAE to IMA angiography, inferior phrenic artery (IPA) involvement with tumor, presence of hepatic artery occlusion, and use of other treatments were compared in groups with and without involvement of the IMA.

RESULTS: The group with IMA involvement included 10 patients; the group without involvement, 20 patients. TAE had been performed two to 12 times in the group with involvement and zero to six times in the group without involvement (P = .01). Mean tumor sizes in these two groups were 5.1 and 6.0 cm, respectively; hepatic artery occlusion was noted in nine and zero patients (P = .01) in the two groups. The time from initial TAE to IMA angiography ranged from 3 to 53 months (median, 31.5 months) and from zero to 89 months (median, 0 months) (P = .01). IPA involvement was observed in seven and four patients (P = .015).

CONCLUSION: These results strongly suggest that, regardless of tumor size, when HCCs are located in the ventral hepatic areas directly beneath the diaphragm, the IMAs serve as feeding arteries in patients with hepatic artery occlusion caused by repeated TAE.

Index terms: Arteries, internal mammary, 949.121, 949.122 • Hepatic arteries, stenosis or obstruction, 952.44 • Liver neoplasms, 761.323 • Liver neoplasms, blood supply • Liver neoplasms, chemotherapeutic embolization, 761.1264

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Since transcatheter arterial embolization (TAE) was reported as a nonsurgical treatment for hepatocellular carcinoma (HCC) by Yamada et al (1) in 1983, it has come to be widely used for the treatment of nonresectable HCC. With the introduction of fatty acid ethyl esters of iodized poppy seed oil (Lipiodol; Guerbet, Roissy, France) as an embolic material and with the availability of microcatheters, embolization of hepatic arteries at the segmental or subsegmental branch level has enabled local control of tumors and long-term survival (2–4).

Therapeutic modalities for HCC other than TAE have also been developed, and these include the use of ethanol (5,6), acetic acid (7), and hot saline (8) injection therapy with ultrasonographic (US) guidance, percutaneous microwave coagulation therapy (9), and radio-frequency ablation (10). However, in patients surviving for a prolonged period, when recurrence resistant to radical treatment (including surgery) develops or when synchronous or asynchronous multiple tumors occur, the number of TAEs increases, and a number of collateral vessels develop. The internal mammary arteries (IMAs) are among such extrahepatic collateral vessels (11). There have been reports of involvement of the IMA with HCC since publication of a case report by Kim et al (12) in 1995 and others (13,14).

In this study, we performed bilateral internal mammary arteriography in 30 patients with HCCs located in the ventral hepatic areas directly beneath the diaphragm to examine involvement of the IMA as a feeding artery for HCC and to determine possible predisposing factors, including the number of previous TAEs, tumor size, time from initial TAE to IMA angiography, involvement of the inferior phrenic artery (IPA), presence of occlusion of the hepatic artery, and use of treatments other than TAE.

	MATERIALS AND METHODS

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The subjects were 30 patients (22 men, eight women; age range, 53–85 years; mean age, 66.1 years; 31 nodes) with HCCs located in the ventral hepatic areas directly beneath the diaphragm—such as segments S2, S3, S4, and S8—who underwent bilateral internal mammary arteriography between April 1996 and March 1999 (Table 1).

Angiography was performed by using a 5-F pigtail catheter (Cook, Bloomington, Ind) for abdominal aortic angiography, a 5-F RC2 catheter (Clinical Supply, Gifu, Japan) for celiac and superior mesenteric arteriography, and a 5-F Michaelson catheter (Cook) for inferior phrenic arteriography. A 5-F Judkins catheter (Clinical Supply) was then inserted into the IMA, and a 3.2-F microcatheter (Tracker-18; Boston Scientific/Target, Boston, Mass) was coaxially inserted into the Judkins catheter. With the use of a 0.016-inch guide wire (GT Wire; Terumo, Tokyo, Japan) with approximately 1 cm of the tip bent into a J shape, the microcatheter was inserted into the distal portion of the IMA along the guide wire. When the Judkins catheter could not be inserted into the IMA, a 5-F Headhunter-1 catheter (H-1; Cook) was placed in the brachiocephalic trunk or left subclavian artery. Then, a 0.016-inch guide wire was inserted into the IMA, and a 3.2-F microcatheter was advanced to the IMA along the guide wire.

Selective angiography of the IMA was performed with contrast medium (iopamidol 300 [Iopamiron 300]; Schering, Bonn, Germany) at an infusion rate of 1.5 mL/sec (total dose, 8 mL) to determine the presence of tumor vessels and tumor staining. Tumor vessels and tumor staining were evaluated by three radiologists (M.N., M.S., N.K.), and they reached a consensus. Patients with positive findings of tumor vessels and tumor staining were regarded as those with IMA involvement, while patients with negative findings of either of these were considered not to have such involvement.

We performed computed tomography (CT) before angiography in all the patients to confirm the location and size of tumors. Maximum tumor diameter was measured as tumor size. Presence of occlusion of the hepatic artery and possible involvement of the IPA with tumor were evaluated at angiography. Results were evaluated by the three radiologists, as for IMA. Information including other treatments, the number of TAEs, and time from initial TAE to IMA angiography was obtained from patient medical charts.

TAE with iodized poppy seed oil was performed through the IMA in all the patients in the group with IMA involvement. CT was performed, and tumor marker (-fetoprotein and PIVKA II) levels were determined before and after TAE with iodized poppy seed oil to evaluate accumulation of the oil in tumors and reduction in tumor marker levels. After TAE of the IMA with iodized poppy seed oil, the patients were followed up for 2 weeks to evaluate the presence of complications. The number of previous TAEs, tumor size, time from initial TAE to IMA angiography, involvement of the IPA, presence of occlusion of the hepatic artery, use of other treatments (percutaneous ethanol injection therapy and surgery) in the groups with and without IMA involvement were compared.

Statistical analysis was performed with use of the Fisher exact test to compare the two groups for the presence of occlusion of the hepatic artery, involvement of the IPA, and use of other treatments. The Wilcoxon-Gehan test was used to compare the groups for the number of previous TAEs and time from initial TAE to IMA angiography, and the Student t test was used to compare the groups for tumor size. P values less than .05 were considered to indicate a statistically significant difference.

	RESULTS

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Internal mammary arteriography revealed tumor staining and tumor vessels in 10 of 30 patients and no tumor staining or tumor vessels in the remaining 20 patients. Therefore, the group with IMA involvement included 10 patients, while the group without involvement included 20 patients (Table 2). Mean tumor size was 5.1 cm in the group with IMA involvement and 6.0 cm in the group without involvement.

View larger version (131K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

View larger version (150K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

View larger version (167K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

View larger version (173K): [in this window] [in a new window] [Download PPT slide]   Figure 1d. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

View larger version (164K): [in this window] [in a new window] [Download PPT slide]   Figure 1e. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

View larger version (147K): [in this window] [in a new window] [Download PPT slide]   Figure 1f. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 1g. Patient 1. HCC in a 71-year-old man. (a, b) Enhanced transverse CT images (arterial dominant phase) show an enhanced recurrent HCC (arrows) in (a) S4 of the liver directly adjacent to the diaphragm and in (b) S2-S3 of the liver. (c) Anteroposterior celiac arteriogram (sixth angiographic examination) demonstrates occlusion (arrow) of the proper hepatic artery. No tumor staining is observed. (d) Anteroposterior right internal mammary arteriogram shows marked tumor staining (arrow). TAE was performed from the location indicated by the arrowhead. (e) Anteroposterior left internal mammary arteriogram shows artery-to-artery anastomosis (arrow) between the left IMA and the left hepatic artery. Tumor staining (arrowheads) is observed in the hepatic left lobe. (f, g) Nonenhanced transverse CT images obtained after TAE of the bilateral IMAs with fatty acid ethyl esters of iodized poppy seed oil show that the oil accumulates in the recurrent HCC (arrows) in liver (f) S4 and (g) S2-S3.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Charnsangavej et al (16) classified hepatic collateral vessels into an intrahepatic group and an extrahepatic group. They noted that extrahepatic collateral vessels originated along the ligament involved in the liver and had developed to a remarkable extent after ligation of the origin of the hepatic artery or TAE and that the IMA was among the extrahepatic collateral vessels. The IMA branches from the subclavian artery, descends along the outside of the sternum of the anterior chest wall, and branches into the mediastinal artery, sternal branch, pericardiacophrenic artery, anterior intercostal artery, musculophrenic artery, and superior epigastric artery (17).

Michels (15) suggested that an ensiform branch exists as a peripheral branch of the IMA distal to the bifurcation of the anterior intercostal artery and that this branch enters the liver from the hepatic falciform ligament and anastomoses with peripheral branches of the middle or left hepatic arteries.

In our patients with involvement of the IMA as well, anastomosis between the IMA and hepatic artery was angiographically detected. The ensiform branch of the IMA enters the liver from the hepatic falciform ligament and therefore probably supplies S2, S3, or S4 lesions in the vicinity of the hepatic falciform ligament.

In our study as well, HCCs located in S8 or S4 were fed by the right IMA (Fig 2), while those located in S2 or S3 were fed by the left IMA. Because a potential anastomosis is present between the IMA and the hepatic artery, when hepatic arterial flow is blocked or reduced by TAE, the IMA should exhibit a relative increase in blood flow and develop as an artery feeding the tumor.

View larger version (189K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Patient 2. HCC in a 61-year-old man. (a) Enhanced transverse CT image (arterial dominant phase) shows an enhanced recurrent HCC (arrows) 3 cm in diameter in S4 of the liver directly adjacent to the ventral part of the diaphragm. (b) Anteroposterior proper hepatic arteriogram (seventh angiographic examination) shows that the left hepatic artery is notably narrowed (arrow). No tumor staining is observed. (c) Anteroposterior right internal mammary arteriogram shows tumor staining (arrow). Arrowhead indicates the feeding artery of the tumor. This HCC is fed by only the right IMA. (d) Nonenhanced transverse CT image obtained after TAE of the right IMA with fatty acid ethyl esters of iodized poppy seed oil shows that the oil accumulates in the recurrent HCC (arrow) in liver S4.

View larger version (186K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Patient 2. HCC in a 61-year-old man. (a) Enhanced transverse CT image (arterial dominant phase) shows an enhanced recurrent HCC (arrows) 3 cm in diameter in S4 of the liver directly adjacent to the ventral part of the diaphragm. (b) Anteroposterior proper hepatic arteriogram (seventh angiographic examination) shows that the left hepatic artery is notably narrowed (arrow). No tumor staining is observed. (c) Anteroposterior right internal mammary arteriogram shows tumor staining (arrow). Arrowhead indicates the feeding artery of the tumor. This HCC is fed by only the right IMA. (d) Nonenhanced transverse CT image obtained after TAE of the right IMA with fatty acid ethyl esters of iodized poppy seed oil shows that the oil accumulates in the recurrent HCC (arrow) in liver S4.

View larger version (186K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Patient 2. HCC in a 61-year-old man. (a) Enhanced transverse CT image (arterial dominant phase) shows an enhanced recurrent HCC (arrows) 3 cm in diameter in S4 of the liver directly adjacent to the ventral part of the diaphragm. (b) Anteroposterior proper hepatic arteriogram (seventh angiographic examination) shows that the left hepatic artery is notably narrowed (arrow). No tumor staining is observed. (c) Anteroposterior right internal mammary arteriogram shows tumor staining (arrow). Arrowhead indicates the feeding artery of the tumor. This HCC is fed by only the right IMA. (d) Nonenhanced transverse CT image obtained after TAE of the right IMA with fatty acid ethyl esters of iodized poppy seed oil shows that the oil accumulates in the recurrent HCC (arrow) in liver S4.

View larger version (183K): [in this window] [in a new window] [Download PPT slide]   Figure 2d. Patient 2. HCC in a 61-year-old man. (a) Enhanced transverse CT image (arterial dominant phase) shows an enhanced recurrent HCC (arrows) 3 cm in diameter in S4 of the liver directly adjacent to the ventral part of the diaphragm. (b) Anteroposterior proper hepatic arteriogram (seventh angiographic examination) shows that the left hepatic artery is notably narrowed (arrow). No tumor staining is observed. (c) Anteroposterior right internal mammary arteriogram shows tumor staining (arrow). Arrowhead indicates the feeding artery of the tumor. This HCC is fed by only the right IMA. (d) Nonenhanced transverse CT image obtained after TAE of the right IMA with fatty acid ethyl esters of iodized poppy seed oil shows that the oil accumulates in the recurrent HCC (arrow) in liver S4.

For tumors located directly beneath the diaphragm, the most likely extrahepatic collateral vessel is the IPA, because the IPA feeds the diaphragm widely and because the diaphragm is adjacent to the liver over a large portion of its extent. The right and left IPAs usually arise separately from the aorta or from the celiac trunk and give rise to anterior and posterior branches. The right and left IPAs run along the inferior surface of the diaphragm, and their branches are in direct contact with the liver in the region in which no parietal peritoneum covers the diaphragm, the bare area of the liver. Portions of liver S1, S2, and S7 form this bare area. The IPA frequently supplies lesions located in these segments (18).

We recommend that IMA angiography be performed for tumors located in the ventral hepatic areas directly beneath the diaphragm in patients with occlusion of the hepatic artery and that IPA angiography be performed for tumors located in dorsal hepatic areas directly adjacent to the diaphragm, such as S1, S2, and S7. The IPA has many anastomotic branches, including the musculophrenic artery and pericardiacophrenic artery of the IMA, the intercostal artery, and subcapsular branches of hepatic arterial branches in the diaphragm (15,19). Therefore, the higher frequency of IPA involvement in the group with IMA involvement compared with that in the group without IMA involvement appeared to be due to the development of these anastomotic branches in the diaphragm with occlusion of the hepatic arterial branches after TAE.

There was no significant difference in tumor size between these two groups, indicating that tumor size is not significantly related to development of the IMA.

In this study, TAE was performed in all 10 patients with involvement of the IMA, without apparent complications; TAE resulted in accumulation of oil in tumor and reduction of tumor marker levels, with good local tumor control. In a report by Kim et al (12) as well, TAE was performed through the IMA in two patients with large HCCs directly beneath the diaphragm and in contact with the anterior abdominal wall; TAE resulted in a marked decrease in tumor marker levels. However, they reported that one of their patients complained of severe pain in the right upper area of the chest for 2 days after TAE. None of our patients complained of chest pain, probably because the microcatheter was advanced to the periphery of the IMA during TAE. Extensive TAE of the IMA may induce necrosis of the anterior thoracic wall or diaphragm. Hence, during TAE of the IMA, the catheter should be advanced to the vicinity of the tumor to selectively embolize tumor vessels.

The results of this study strongly suggest that, regardless of tumor size, when HCC is located in the ventral hepatic areas directly beneath the diaphragm, the IMAs serve as feeding arteries in patients who survive for a prolonged period and exhibit occlusion of the hepatic artery caused by repeated TAE.

	FOOTNOTES

 
Abbreviations: HCC = hepatocellular carcinoma, IMA = internal mammary artery, IPA = inferior phrenic artery, PIVKA II = protein induced by vitamin K absence II, TAE = transcatheter arterial embolization

Author contributions: Guarantor of integrity of entire study, M.S.; study concepts and design, M.N.; definition of intellectual content, T.T.; literature research, N.K.; clinical studies, M.N.; data acquisition and analysis, M.N.; statistical analysis, K.K.; manuscript preparation, M.T.; manuscript editing, H.T.; manuscript review, M.M.; manuscript final version approval, H.M.

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