DOI: 10.1148/rg.25si055508
RadioGraphics 2005;25:S25-S39
© RSNA, 2005
Recognizing Extrahepatic Collateral Vessels That Supply Hepatocellular Carcinoma to Avoid Complications of Transcatheter Arterial Chemoembolization1
Hyo-Cheol Kim, MD,
Jin Wook Chung, MD,
Whal Lee, MD,
Hwan Jun Jae, MD and
Jae Hyung Park, MD
1 From the Department of Radiology, Seoul National University College of Medicine, and the Institute of Radiation Medicine, Seoul National University Medical Research Center, and Clinical Research Institute, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea. Recipient of a Cum Laude award for an education exhibit at the 2004 RSNA Annual Meeting. Received February 8, 2005; accepted March 23. All authors have no financial relationships to disclose.
Address correspondence to J.W.C. (e-mail: chungjw{at}radcom.snu.ac.kr).
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Abstract
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Extrahepatic collateral arteries commonly supply hepatocellular carcinomas if the tumors are large or peripherally located. Because development of these vessels interferes with effective control of the tumor with transcatheter arterial chemoembolization (TACE), radiologists should become familiar with the imaging findings of extrahepatic collateral vessels to detect them at an early stage. The authors observed 2104 such vessels in 860 patients over 5.5 years. The extrahepatic collateral vessels observed originated from the inferior phrenic artery, omental branch, adrenal artery, intercostal artery, cystic artery, internal mammary artery, renal or renal capsular artery, branch of the superior mesenteric artery, gastric artery, and lumbar artery. The authors suspected extrahepatic collateral vessels when (a) a tumor grew exophytically or invaded adjacent organs, (b) a tumor was in contact with the ligaments and bare area of the liver, (c) a hypertrophied extrahepatic collateral vessel was observed on a computed tomographic (CT) scan, (d) a peripheral defect of iodized oil retention within a tumor was seen during chemoembolization or on a follow-up CT scan, (e) a local recurrence developed at the peripheral portion of the treated tumor during follow-up, or (f) a sustained elevation in serum 
-fetoprotein level was noted despite adequate embolization of the hepatic artery. When both the hepatic artery and extrahepatic collateral vessels supply a tumor, additional extrahepatic collateral vessel chemoembolization should be attempted to increase the therapeutic efficacy of TACE for hepatocellular carcinoma.
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LEARNING OBJECTIVES
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After reading this article and taking the test, the reader will be able to:
- Identify the spectrum of extrahepatic collateral vessels that supply hepatocellular carcinoma.
- Describe typical radiologic findings of extrahepatic collateral vessels that supply hepatocellular carcinoma at initial CT, angiography, and follow-up CT.
- Discuss when and how to perform chemoembolization via extrahepatic collateral vessels.
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Introduction
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Transcatheter arterial chemoembolization (TACE) is widely used to manage unresectable hepatocellular carcinoma (HCC) and has become accepted as a good alternative to hepatic surgery (1–3). HCC chemoembolization is based on the fact that the normal liver parenchyma receives a dual blood supply from the hepatic artery and the portal vein, whereas HCCs are supplied exclusively by the hepatic artery. In practice, we frequently encounter HCCs supplied by extrahepatic collateral arteries even when the hepatic artery is patent (4,5). Moreover, the development of extrahepatic collateral arteries that supply HCC interferes with effective control of the tumor with TACE. To detect these vessels at an early stage, interventional radiologists should be familiar with the spectrum of extrahepatic collateral vessels that supply HCC, the factors that lead to their formation, and their characteristic imaging appearance at computed tomographic (CT) and conventional angiography. These topics are discussed herein, as well as ways in which to avoid complications of TACE of the collateral vessels.
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Extrahepatic Collateral Vessels That Supply HCC
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From January 1998 to July 2003, 9618 sessions of TACE were performed in 3179 patients with HCC at our institution. Selective angiography was performed in almost all cases with extrahepatic collateral arteries suspected of supplying HCCs. We observed 2104 extrahepatic collateral routes in 1622 sessions in 860 patients (27%) and performed TACE via 1556 extrahepatic collateral vessels (74%) in 732 patients (1281 sessions). Multiple extrahepatic collateral vessels were embolized in 221 patients (two vessels in 186 patients, three vessels in 27, four vessels in six, and five vessels in two). The frequency of the extrahepatic collateral vessels observed and embolized in our patient series are listed in the Table and their locations are shown schematically in Figure 1. Considering the broad contact between the liver and the diaphragm, it may be expected that diaphragmatic blood supplies, including the inferior phrenic, internal mammary, and intercostal arteries, are the major sources of collateral circulation. Exophytic growth and extracapsular HCC infiltration can cause omental adhesion. Direct contact or invasion into other organs, including the stomach, colon, adrenal gland, and kidney, may create blood supply to the tumor from these organs.
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Figure 1. Diagram illustrates the potential extrahepatic collateral arteries that supply HCCs according to anatomic location. 1 = internal mammary artery, 2 = pericardiophrenic artery, 3 = musculophrenic artery, 4 = inferior phrenic artery, 5 = superior adrenal artery, 6 = inferior adrenal artery, 7 = superior renal capsular artery, 8 = omental branch, 9 = colic branch, 10 = intercostal artery, 11 = left gastric artery, 12 = gastroepiploic artery.
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Inferior Phrenic Artery
The right inferior phrenic artery (Figs 2–5) was found to be the most common extrahepatic collateral vessel that supplies HCC. The inferior phrenic artery supplies most of the diaphragm, including the area in contact with the bare area of the liver, and anastomoses with the adjacent arteries, including the internal mammary, intercostal, and adrenal arteries. The right and the left inferior phrenic arteries usually originate from the celiac trunk or directly from the aorta as a common trunk or independent origins (6). Less frequently, they arise from the renal arteries (Fig 5c) or, rarely, from the left gastric or hepatic arteries. On arterial phase computed tomographic (CT) scans, we can frequently identify the vertical segment of the hypertrophied inferior phrenic artery (Fig 2a) and guess its origin (5,7). In this era of thin-section multi–detector row CT, the origin can be directly viewed in most cases.
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Figure 2a. HCC supplied by the left inferior phrenic artery in a 60-year-old woman. (a) Transverse CT scan shows an exophytic mass (arrowheads) in the left hepatic lobe. (b) Left inferior phrenic arteriogram shows a hypervascular tumor (arrow). There was no tumor staining on the hepatic arteriogram (not shown).
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Figure 2b. HCC supplied by the left inferior phrenic artery in a 60-year-old woman. (a) Transverse CT scan shows an exophytic mass (arrowheads) in the left hepatic lobe. (b) Left inferior phrenic arteriogram shows a hypervascular tumor (arrow). There was no tumor staining on the hepatic arteriogram (not shown).
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Figure 3a. HCC supplied by the right inferior phrenic artery in a 56-year-old man. (a) Transverse CT scan shows a huge mass (M) at the dome of the right hepatic lobe. Note the hypertrophied right inferior phrenic artery (arrow). (b) Celiac arteriogram from the first session of TACE shows a huge hypervascular mass. Note faint tumor staining in the superolateral portion (arrowheads) of the tumor. (c) Right inferior phrenic arteriogram shows hypervascular tumor staining that corresponds to the faint staining seen on the celiac arteriogram.
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Figure 3b. HCC supplied by the right inferior phrenic artery in a 56-year-old man. (a) Transverse CT scan shows a huge mass (M) at the dome of the right hepatic lobe. Note the hypertrophied right inferior phrenic artery (arrow). (b) Celiac arteriogram from the first session of TACE shows a huge hypervascular mass. Note faint tumor staining in the superolateral portion (arrowheads) of the tumor. (c) Right inferior phrenic arteriogram shows hypervascular tumor staining that corresponds to the faint staining seen on the celiac arteriogram.
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Figure 3c. HCC supplied by the right inferior phrenic artery in a 56-year-old man. (a) Transverse CT scan shows a huge mass (M) at the dome of the right hepatic lobe. Note the hypertrophied right inferior phrenic artery (arrow). (b) Celiac arteriogram from the first session of TACE shows a huge hypervascular mass. Note faint tumor staining in the superolateral portion (arrowheads) of the tumor. (c) Right inferior phrenic arteriogram shows hypervascular tumor staining that corresponds to the faint staining seen on the celiac arteriogram.
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Figure 4a. HCC supplied by the right inferior phrenic artery in a 49-year-old man. (a) Transverse CT scan obtained after two sessions of TACE shows a defect in iodized oil retention and enhancement of the defect portion, findings that indicate viable tumor (arrowhead). (b) Right inferior phrenic arteriogram shows hypervascular staining (straight arrow) within the tumor retaining iodized oil. Note normal adrenal gland staining (arrowhead) and the superior adrenal artery (curved arrow).
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Figure 4b. HCC supplied by the right inferior phrenic artery in a 49-year-old man. (a) Transverse CT scan obtained after two sessions of TACE shows a defect in iodized oil retention and enhancement of the defect portion, findings that indicate viable tumor (arrowhead). (b) Right inferior phrenic arteriogram shows hypervascular staining (straight arrow) within the tumor retaining iodized oil. Note normal adrenal gland staining (arrowhead) and the superior adrenal artery (curved arrow).
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Figure 5a. HCC supplied by the right inferior phrenic artery after repeated TACE via the hepatic artery in a 62-year-old man. (a) Transverse CT scan obtained after seven sessions of TACE shows a recurrent tumor (arrow) in the right hepatic lobe. (b) Celiac arteriogram from the eighth session of TACE shows an attenuated right hepatic artery (arrow) and no tumor staining. (c) Inferior phrenic arteriogram shows a hypervascular mass (arrow). Note the inferior phrenic artery originating from the right renal artery and normal parenchymal staining of the upper pole of the right kidney (arrowhead).
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Figure 5b. HCC supplied by the right inferior phrenic artery after repeated TACE via the hepatic artery in a 62-year-old man. (a) Transverse CT scan obtained after seven sessions of TACE shows a recurrent tumor (arrow) in the right hepatic lobe. (b) Celiac arteriogram from the eighth session of TACE shows an attenuated right hepatic artery (arrow) and no tumor staining. (c) Inferior phrenic arteriogram shows a hypervascular mass (arrow). Note the inferior phrenic artery originating from the right renal artery and normal parenchymal staining of the upper pole of the right kidney (arrowhead).
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Figure 5c. HCC supplied by the right inferior phrenic artery after repeated TACE via the hepatic artery in a 62-year-old man. (a) Transverse CT scan obtained after seven sessions of TACE shows a recurrent tumor (arrow) in the right hepatic lobe. (b) Celiac arteriogram from the eighth session of TACE shows an attenuated right hepatic artery (arrow) and no tumor staining. (c) Inferior phrenic arteriogram shows a hypervascular mass (arrow). Note the inferior phrenic artery originating from the right renal artery and normal parenchymal staining of the upper pole of the right kidney (arrowhead).
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When the tumor is located in liver segment S7 and is in contact with the right hemidiaphragm, selective angiography of the right inferior phrenic artery is mandatory. When the tumor is located in liver segments S2 or S3 and abuts the left hemidiaphragm, the possibility of a collateral blood supply from the left inferior phrenic artery should be kept in mind. Patients commonly complain of shoulder pain or chest tightness during embolization of the inferior phrenic artery.
Internal Mammary Artery
The internal mammary artery arises from the proximal part of the subclavian artery, opposite the origin of the vertebral artery. It supplies the far anterior aspect of the diaphragm and gives off anterior intercostal branches, the pericardiophrenic artery, anterior mediastinal arteries, pericardial branches, and sternal branches. The pericardiophrenic artery typically anastomoses with the inferior phrenic artery. At the level of the sixth intercostal space, the internal mammary artery divides into the musculophrenic artery and the superior epigastric artery. The musculophrenic artery passes obliquely downward and laterally, behind the seventh, eighth, and ninth costal cartilages. It perforates the diaphragm near the ninth costal cartilage and terminates opposite the last intercostal space. It gives off two anterior intercostal branches to each of the seventh, eighth, and ninth intercostal spaces and anastomoses with the inferior phrenic artery. The superior epigastric artery gives off some branches to the diaphragm, which extend into the falciform ligament of the liver and anastomose with the hepatic artery (8).
Regardless of the patency of the hepatic artery, when an HCC is located in ventral hepatic areas, abutting the diaphragm and anterior abdominal wall, the internal mammary arteries may serve as feeding arteries (4,9). HCCs located in liver segments S8 or S4 are fed by the right internal mammary artery (Fig 6), whereas those located in the left lateral segment are fed by the left internal mammary artery (Fig 7). In our experience, the pericardiophrenic artery supplies HCCs in about two-thirds of patients, and the musculophrenic artery supplies them in about one-third. The superior epigastric and anterior intercostal arteries rarely supply tumors.
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Figure 6a. HCC supplied by the right internal mammary artery in a 55-year-old man who had undergone S2 segmentectomy. (a) Transverse CT scan obtained after the 11th session of postoperative TACE shows a recurrent tumor of the ventral aspect of segment S4 (arrows). (b) Oblique right internal mammary arteriogram shows tumor staining, mainly supplied by the pericardiophrenic artery (arrow). The musculophrenic artery (arrowhead) is also seen.
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Figure 6b. HCC supplied by the right internal mammary artery in a 55-year-old man who had undergone S2 segmentectomy. (a) Transverse CT scan obtained after the 11th session of postoperative TACE shows a recurrent tumor of the ventral aspect of segment S4 (arrows). (b) Oblique right internal mammary arteriogram shows tumor staining, mainly supplied by the pericardiophrenic artery (arrow). The musculophrenic artery (arrowhead) is also seen.
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Figure 7a. HCC supplied by the left internal mammary artery in a 63-year-old man. (a) Transverse CT scan obtained after three sessions of TACE shows a large tumor (arrows) directly adjacent to the ventral part of the diaphragm. (b) Left internal mammary arteriogram shows tumor staining supplied by the branch of the internal mammary artery (straight arrow). Note the superior epigastric artery (arrowhead) and musculophrenic artery (curved arrow).
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Figure 7b. HCC supplied by the left internal mammary artery in a 63-year-old man. (a) Transverse CT scan obtained after three sessions of TACE shows a large tumor (arrows) directly adjacent to the ventral part of the diaphragm. (b) Left internal mammary arteriogram shows tumor staining supplied by the branch of the internal mammary artery (straight arrow). Note the superior epigastric artery (arrowhead) and musculophrenic artery (curved arrow).
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Intercostal and Lumbar Arteries
There are nine pairs of posterior intercostal arteries that originate from the dorsal aspect of the thoracic aorta. They anastomose with the anterior intercostal branches of the internal mammary artery after giving off the dorsal branch, the collateral intercostal branch, and the muscular branch. Lower posterior intercostal arteries anastomose with the inferior phrenic artery at the insertion site of the diaphragm. A hypertrophied intercostal artery may be observed as a dotlike or linear structure just inferior to the ribs on arterial phase CT scans (10).
HCCs abutting the inferolateral aspect of the diaphragm are frequently supplied by the posterior intercostal arteries (Fig 8 ). HCCs invading the abdominal wall were also found to be supplied by the lower intercostal, subcostal, or lumbar arteries (Fig 9). The intercostal artery always passed the diaphragm insertion site to supply the HCC, abutting the diaphragm and making a sharp upward turn near the costochondral junction (10). A microcatheter should be advanced beyond the diaphragmatic insertion to the thoracic cage, where a sharp upward turn is seen, to avoid possible complications such as skin necrosis and spinal infarction (10). The common levels of the intercostal arteries that supply HCCs are T10, T9, and T11, in order of frequency (10). Occasionally, HCCs that abut the posteroinferior diaphragm can be supplied by the subcostal or lumbar arteries.
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Figure 8a. HCC supplied by the intercostal artery in a 46-year-old man. (a) Transverse CT scan obtained after the first session of TACE shows disseminated tumor in the liver, particularly in the right hepatic lobe. Note the focal obscured margin (arrowhead) between the liver and chest wall. (b) Celiac arteriogram from the second session of TACE shows a diffuse hypervascular tumor of the liver and a focal defect (arrowheads) in tumor staining. (c) Intercostal arteriogram shows the 10th intercostal artery, which supplies the defect portion of the tumor. Note the sharp upward turn (arrow) of the vessels feeding the tumor.
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Figure 8b. HCC supplied by the intercostal artery in a 46-year-old man. (a) Transverse CT scan obtained after the first session of TACE shows disseminated tumor in the liver, particularly in the right hepatic lobe. Note the focal obscured margin (arrowhead) between the liver and chest wall. (b) Celiac arteriogram from the second session of TACE shows a diffuse hypervascular tumor of the liver and a focal defect (arrowheads) in tumor staining. (c) Intercostal arteriogram shows the 10th intercostal artery, which supplies the defect portion of the tumor. Note the sharp upward turn (arrow) of the vessels feeding the tumor.
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Figure 8c. HCC supplied by the intercostal artery in a 46-year-old man. (a) Transverse CT scan obtained after the first session of TACE shows disseminated tumor in the liver, particularly in the right hepatic lobe. Note the focal obscured margin (arrowhead) between the liver and chest wall. (b) Celiac arteriogram from the second session of TACE shows a diffuse hypervascular tumor of the liver and a focal defect (arrowheads) in tumor staining. (c) Intercostal arteriogram shows the 10th intercostal artery, which supplies the defect portion of the tumor. Note the sharp upward turn (arrow) of the vessels feeding the tumor.
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Figure 9a. HCC supplied by the lumbar artery in a 55-year-old man. (a) Transverse CT scan shows a huge exophytic mass with partial uptake of iodized oil. Note the tumor invasion of the right abdominal wall (arrowheads) and omental infiltration around the tumor. (b) Gastroduodenal arteriogram shows a large area of tumor staining (arrowheads) supplied by the omental branch. (c) Abdominal aortogram shows the engorged lumbar artery (arrow) supplying the tumor stain.
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Figure 9b. HCC supplied by the lumbar artery in a 55-year-old man. (a) Transverse CT scan shows a huge exophytic mass with partial uptake of iodized oil. Note the tumor invasion of the right abdominal wall (arrowheads) and omental infiltration around the tumor. (b) Gastroduodenal arteriogram shows a large area of tumor staining (arrowheads) supplied by the omental branch. (c) Abdominal aortogram shows the engorged lumbar artery (arrow) supplying the tumor stain.
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Figure 9c. HCC supplied by the lumbar artery in a 55-year-old man. (a) Transverse CT scan shows a huge exophytic mass with partial uptake of iodized oil. Note the tumor invasion of the right abdominal wall (arrowheads) and omental infiltration around the tumor. (b) Gastroduodenal arteriogram shows a large area of tumor staining (arrowheads) supplied by the omental branch. (c) Abdominal aortogram shows the engorged lumbar artery (arrow) supplying the tumor stain.
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Omental Branch
The omental branch (Figs 10, 11) from the gastroepiploic artery (or in rare cases from the dorsal pancreatic artery) is the second most common collateral vessel. Whereas most of the other extrahepatic collateral vessels enter the liver via the suspensory ligament or bare area of the liver, the omental branch supplies the tumor by direct adhesion to the omentum.
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Figure 10a. HCC supplied by the omental branch in a 42-year-old man who had undergone right lobectomy of the liver. (a) Transverse CT scan shows multiple small enhancing nodules in the liver. (b) Celiac arteriogram shows multiple hypervascular nodules in the liver. Note the prominent omental branch (arrow).
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Figure 10b. HCC supplied by the omental branch in a 42-year-old man who had undergone right lobectomy of the liver. (a) Transverse CT scan shows multiple small enhancing nodules in the liver. (b) Celiac arteriogram shows multiple hypervascular nodules in the liver. Note the prominent omental branch (arrow).
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Figure 11a. HCC supplied by the omental branches in a 57-year-old man. (a) Transverse CT scan obtained after 14 sessions of TACE shows multiple enhancing masses in the liver. Note prominent omental vessels (arrowhead) around the liver. The spleen (S) is also seen. (b) Gastroduodenal arteriogram obtained at the 15th session of TACE shows two prominent omental branches (arrowheads) supplying a hypervascular mass. (c) Radiograph obtained at TACE shows a microcatheter (arrowheads) inserted in the omental branch passed over the gastroduodenal and right gastroepiploic arteries. Arrow = microcatheter tip.
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Figure 11b. HCC supplied by the omental branches in a 57-year-old man. (a) Transverse CT scan obtained after 14 sessions of TACE shows multiple enhancing masses in the liver. Note prominent omental vessels (arrowhead) around the liver. The spleen (S) is also seen. (b) Gastroduodenal arteriogram obtained at the 15th session of TACE shows two prominent omental branches (arrowheads) supplying a hypervascular mass. (c) Radiograph obtained at TACE shows a microcatheter (arrowheads) inserted in the omental branch passed over the gastroduodenal and right gastroepiploic arteries. Arrow = microcatheter tip.
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Figure 11c. HCC supplied by the omental branches in a 57-year-old man. (a) Transverse CT scan obtained after 14 sessions of TACE shows multiple enhancing masses in the liver. Note prominent omental vessels (arrowhead) around the liver. The spleen (S) is also seen. (b) Gastroduodenal arteriogram obtained at the 15th session of TACE shows two prominent omental branches (arrowheads) supplying a hypervascular mass. (c) Radiograph obtained at TACE shows a microcatheter (arrowheads) inserted in the omental branch passed over the gastroduodenal and right gastroepiploic arteries. Arrow = microcatheter tip.
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Omental branches usually are small and branch at an acute angle from the gastroepiploic artery. Several omental branches exist in healthy patients, but they are hardly recognized on angiograms. However, when an omental branch supplies an HCC, it becomes sufficiently dilated to be recognizable at celiac angiography (11,12). Therefore, a careful review of celiac angiograms is a first step toward detecting the omental branch that supplies an HCC. In patients with a ruptured HCC, hemostasis can be achieved with TACE through the omental branch (11).
Because the greater omentum is remarkably mobile, the omental branch can supply a tumor in any intraperitoneal portion of the liver. In patients with severe liver cirrhosis, the liver shrinks so markedly that an exophytic tumor in the liver dome can be supplied by an omental branch with a very long path.
Adrenal Artery
If a tumor extends inferomedially, adrenal arteries can supply the tumor (Figs 12, 13). The adrenal gland has three sources of arterial supply: a superior adrenal artery that arises from the inferior phrenic artery, a middle adrenal artery that arises from the lateral aspect of the aorta at a level between the celiac and renal arteries, and an inferior adrenal artery that arises from the superior aspect of the ipsilateral renal artery. Normal adrenal gland staining is triangular. On inferior phrenic angiograms (Fig 5b), superior adrenal artery and normal adrenal gland staining are usually observed. Therefore, normal adrenal gland staining must not be confused with tumor staining on inferior phrenic angiograms.
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Figure 12a. HCC supplied by the superior adrenal artery in a 56-year-old man. (a) Transverse CT scan obtained after 19 sessions of TACE shows a viable tumor (arrow) in the inferomedial portion of the right hepatic lobe. (b) Inferior phrenic arteriogram obtained at the 20th session of TACE shows the hypervascular mass supplied by the superior adrenal artery (arrow).
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Figure 12b. HCC supplied by the superior adrenal artery in a 56-year-old man. (a) Transverse CT scan obtained after 19 sessions of TACE shows a viable tumor (arrow) in the inferomedial portion of the right hepatic lobe. (b) Inferior phrenic arteriogram obtained at the 20th session of TACE shows the hypervascular mass supplied by the superior adrenal artery (arrow).
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Figure 13a. HCC supplied by the adrenal artery in a 62-year-old man. (a) Transverse CT scan shows a large tumor (M) abutting the inferior vena cava. (b) Celiac arteriogram shows a hypervascular tumor (arrows). (c) On an unenhanced transverse CT scan obtained after the first TACE session, iodized oil was not retained in the medial portion of the tumor (arrow). (d) Adrenal arteriogram obtained at the second session of TACE shows the hypervascular tumor (arrow). Unenhanced CT scan obtained after the second session of TACE (not shown) demonstrated additional retention of iodized oil in the medial portion of the tumor.
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Figure 13b. HCC supplied by the adrenal artery in a 62-year-old man. (a) Transverse CT scan shows a large tumor (M) abutting the inferior vena cava. (b) Celiac arteriogram shows a hypervascular tumor (arrows). (c) On an unenhanced transverse CT scan obtained after the first TACE session, iodized oil was not retained in the medial portion of the tumor (arrow). (d) Adrenal arteriogram obtained at the second session of TACE shows the hypervascular tumor (arrow). Unenhanced CT scan obtained after the second session of TACE (not shown) demonstrated additional retention of iodized oil in the medial portion of the tumor.
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Figure 13c. HCC supplied by the adrenal artery in a 62-year-old man. (a) Transverse CT scan shows a large tumor (M) abutting the inferior vena cava. (b) Celiac arteriogram shows a hypervascular tumor (arrows). (c) On an unenhanced transverse CT scan obtained after the first TACE session, iodized oil was not retained in the medial portion of the tumor (arrow). (d) Adrenal arteriogram obtained at the second session of TACE shows the hypervascular tumor (arrow). Unenhanced CT scan obtained after the second session of TACE (not shown) demonstrated additional retention of iodized oil in the medial portion of the tumor.
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Figure 13d. HCC supplied by the adrenal artery in a 62-year-old man. (a) Transverse CT scan shows a large tumor (M) abutting the inferior vena cava. (b) Celiac arteriogram shows a hypervascular tumor (arrows). (c) On an unenhanced transverse CT scan obtained after the first TACE session, iodized oil was not retained in the medial portion of the tumor (arrow). (d) Adrenal arteriogram obtained at the second session of TACE shows the hypervascular tumor (arrow). Unenhanced CT scan obtained after the second session of TACE (not shown) demonstrated additional retention of iodized oil in the medial portion of the tumor.
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Renal and Renal Capsular Arteries
If a tumor extends posteroinferiorly, it may be fed by the renal and renal capsular arteries (Fig 14). The superior capsular artery usually arises together with the inferior adrenal artery from the renal artery and follows a characteristic tortuous path over the superior pole of the kidney. Perforating capsular arteries arise from arcuate and interlobular arteries, which are branches of the renal artery. In advanced cases of HCC, multiple arteries supply the tumor, and it may be difficult to differentiate the renal capsular artery, renal artery, and inferior adrenal artery.
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Figure 14a. HCC supplied by the renal arteries in a 51-year-old man. (a) Transverse CT scan obtained after the third session of TACE shows an exophytic mass (M) in the tip of the right hepatic lobe, compressing the right kidney. (b) Right renal arteriogram shows tumor staining (arrowhead) supplied by renal arteries and a prominent superior renal capsular artery (arrow).
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Figure 14b. HCC supplied by the renal arteries in a 51-year-old man. (a) Transverse CT scan obtained after the third session of TACE shows an exophytic mass (M) in the tip of the right hepatic lobe, compressing the right kidney. (b) Right renal arteriogram shows tumor staining (arrowhead) supplied by renal arteries and a prominent superior renal capsular artery (arrow).
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Superior Mesenteric Artery
Because of exophytic growth and extracapsular infiltration, an HCC may have direct contact with the intraabdominal organs, such as the colon and stomach. When an exophytic tumor is located in the inferior tip of the right hepatic lobe, the hepatic flexure of the colon can be in close contact with the tumor. A branch of the superior mesenteric artery, particularly the colic branch, may supply the tumor under these conditions (Fig 15).
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Figure 15a. HCC supplied by the colic branch of the superior mesenteric artery in a 55-year-old man. (a) Transverse CT scan obtained after the third session of TACE shows an exophytic mass (arrow) with partial iodized oil retention in the right hepatic lobe. (b) Celiac arteriogram shows some tumor staining supplied by the hepatic artery and omental branch from the gastroduodenal artery. Note the large defect of tumor staining (*). (c) Selective angiogram of the colic branch shows vessels supplying the tumor (arrowhead) and tumor staining (arrow) corresponding to the tumor staining defect in seen b.
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Figure 15b. HCC supplied by the colic branch of the superior mesenteric artery in a 55-year-old man. (a) Transverse CT scan obtained after the third session of TACE shows an exophytic mass (arrow) with partial iodized oil retention in the right hepatic lobe. (b) Celiac arteriogram shows some tumor staining supplied by the hepatic artery and omental branch from the gastroduodenal artery. Note the large defect of tumor staining (*). (c) Selective angiogram of the colic branch shows vessels supplying the tumor (arrowhead) and tumor staining (arrow) corresponding to the tumor staining defect in seen b.
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Figure 15c. HCC supplied by the colic branch of the superior mesenteric artery in a 55-year-old man. (a) Transverse CT scan obtained after the third session of TACE shows an exophytic mass (arrow) with partial iodized oil retention in the right hepatic lobe. (b) Celiac arteriogram shows some tumor staining supplied by the hepatic artery and omental branch from the gastroduodenal artery. Note the large defect of tumor staining (*). (c) Selective angiogram of the colic branch shows vessels supplying the tumor (arrowhead) and tumor staining (arrow) corresponding to the tumor staining defect in seen b.
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Gastric Artery
When an HCC has broad contact with the stomach, the gastric artery can supply the tumor (Fig 16). The left gastric artery usually arises from the celiac axis and rarely from the supraceliac aorta. The right gastric artery commonly arises from the proper hepatic and left hepatic arteries and infrequently arises from the gastroduodenal and common hepatic arteries. Normal stomach staining can often mimic tumor staining. To prevent inadvertent embolization of the stomach, selective catheterization should be attempted, but this technique cannot be accomplished in many cases. Therefore, embolization of the gastric artery is infrequently performed.
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Figure 16a. HCC supplied by the left gastric artery in a 62-year-old woman. (a) Transverse CT scan obtained after the 18th session of TACE shows a viable tumor (arrow) with partial retention of iodized oil that abuts the stomach in the left hepatic lobe. (b) Left gastric arteriogram shows multiple tumor staining (arrows) and normal stomach staining (arrowheads).
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Figure 16b. HCC supplied by the left gastric artery in a 62-year-old woman. (a) Transverse CT scan obtained after the 18th session of TACE shows a viable tumor (arrow) with partial retention of iodized oil that abuts the stomach in the left hepatic lobe. (b) Left gastric arteriogram shows multiple tumor staining (arrows) and normal stomach staining (arrowheads).
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Cystic Artery
The cystic artery is the first branch of the right hepatic artery and usually supplies the liver parenchyma near the gallbladder bed. When the tumor protrudes to the gallbladder fossa, it may be supplied by the cystic artery (Fig 17), despite an intact hepatic artery. When hepatic arteries are attenuated because of repeated TACE, a tumor located at a distance from the gallbladder fossa may be fed by the cystic artery. Embolization of the cystic artery may cause cholecystitis or gallbladder infarction, but TACE after selective catheterization into the tumor-feeding branch is usually safe (13).
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Figure 17a. HCC supplied by the cystic artery in a 49-year-old man. (a) Transverse CT scan shows a tumor in the gallbladder fossa (arrowheads). Arrow = gallbladder. (b) As seen on the cystic arteriogram, part of the tumor (arrow) in the gallbladder fossa was supplied by the cystic artery. (c) Radiograph obtained at TACE shows retention of iodized oil. Note the microcatheter (arrowheads) inserted in the tumor-feeding branch.
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Figure 17b. HCC supplied by the cystic artery in a 49-year-old man. (a) Transverse CT scan shows a tumor in the gallbladder fossa (arrowheads). Arrow = gallbladder. (b) As seen on the cystic arteriogram, part of the tumor (arrow) in the gallbladder fossa was supplied by the cystic artery. (c) Radiograph obtained at TACE shows retention of iodized oil. Note the microcatheter (arrowheads) inserted in the tumor-feeding branch.
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Figure 17c. HCC supplied by the cystic artery in a 49-year-old man. (a) Transverse CT scan shows a tumor in the gallbladder fossa (arrowheads). Arrow = gallbladder. (b) As seen on the cystic arteriogram, part of the tumor (arrow) in the gallbladder fossa was supplied by the cystic artery. (c) Radiograph obtained at TACE shows retention of iodized oil. Note the microcatheter (arrowheads) inserted in the tumor-feeding branch.
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In advanced cases of HCC, the cystic artery frequently supplies the tumor because of its vicinity. In our patient series, the prevalence of cystic arterial supply to HCC was markedly underestimated because selective angiography of cystic artery had not been routinely performed in advanced cases, and, as a result, the high performance rate of chemoembolization was also overestimated.
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Causes of Extrahepatic Collateral Vessel Formation
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In the past, the main cause of extrahepatic collateral vessel development was believed to be hepatic artery occlusion by surgical ligation, a procedure that is no longer performed (14,15). Some authors advocate that hepatic artery interruption by repeated TACE or arterial dissection is the primary cause (9,16). In our experience, however, only about 4% of patients had proximal hepatic artery occlusion, and most patients with a collateral supply had a widely patent hepatic artery (5). The anatomic location of the tumor adjacent to the bare area and suspensory ligaments of the liver and direct invasion of or adhesions to adjacent organs seem to be primary causes. Attenuation or occlusion of the hepatic artery may exaggerate the degree of collateral circulation. Repeated TACE and the resultant obliteration of peripheral hepatic arteries is also an important cause of collateral vessel formation, particularly for recurrent tumors. A previous abdominal operation may predispose a patient to early formation of collateral vessels to a tumor due to postoperative omental or peritoneal adhesion. In cases of recurrent tumor at the resection margin, collateral supply from omental arteries should be considered. Peripheral hepatic infarction after TACE sometimes induces omental or peritoneal adhesion, and extrahepatic collateral vessels can develop through the adhesion.
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Radiologic Findings at CT and Angiography
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Because selective angiography of individual collateral vessels is tedious and time consuming, it is essential to try to determine first whether parasitic or collateral blood supply is present. The initial CT scan provides useful information, and CT signs of direct invasion into adjacent organs or extracapsular infiltration indicate the presence of extrahepatic collateral vessels (Fig 9a ). Tumors with an exophytic growth pattern are prone to collateral vessels development. If a tumor is in contact with the ligaments and bare area of the liver, there is a high chance of parasitic supply from extrahepatic collateral vessels even in small tumors (Fig 4a). It is sometimes possible to observe hypertrophied extrahepatic collateral vessels, especially the right inferior phrenic artery (Fig 2a), during the arterial phase of helical CT.
Follow-up CT scans are also useful. A peripheral iodized oil retention defect within the tumor or delayed development of viable tumor at the peripheral portion of the treated tumor at follow-up CT indicates the presence of extrahepatic collateral vessels (Fig 5a). In a tumor that recurs after surgery at the resection margin, the presence of omental collateral vessels should be suspected and investigated (Fig 11).
The correlation of CT and angiographic findings is essential. If a tumor observed at CT is not demonstrated at hepatic angiography, collateral vessels must be investigated. When tumor staining on hepatic angiograms has a focal defect or a focal iodized oil retention defect is noted during iodized oil infusion, alternative feeder vessels are a possibility. A hypertrophic omental branch may be noted on celiac angiograms. If the serum -fetoprotein level is persistently elevated even after successful devascularization of the hepatic artery, we recommend an investigation of extrahepatic collateral vessels to the liver.
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Management of Potential Complications of TACE of Extrahepatic Collateral Vessels
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When collateral vessels are chemoembolized, there is a risk of embolizing nontarget branches, which can lead to a variety of complications, depending on location. Cutaneous problems, such as itching, erythema, and necrosis, may arise when the internal mammary, intercostal, or lumbar artery is embolized (17,18). Gastrointestinal erosion, ulceration, or perforation can be caused by gastric, omental, and colic branch artery embolization (19). Paraplegia may result from the inadvertent embolization of spinal branches arising from intercostal or lumbar collateral vessels, and embolization of the cystic artery may cause cholecystitis or gallbladder infarction (20). Chemoembolization of the inferior phrenic artery may result in shoulder pain, pleural effusion, or basal atelectasis (5).
To avoid these complications, selective catheterization should be achieved by placing the catheter tip as close as possible to the specific branch or branches supplying a neoplasm (Fig 17c). Second, embolic materials should be infused incrementally to prevent embolic materials from refluxing into a nontarget branch. Third, coils and gelatin sponge particles may be used to occlude and protect the territory of the normal distal branches before chemoembolization. Fourth, to reduce shoulder pain, it is recommended that a small amount of 1% lidocaine be injected intraarterially during embolization of the inferior phrenic artery.
Because terminal branches of adjacent extrahepatic collateral vessels are anastomosed to each other, multiple collateral vessels can supply one tumor. If an extrahepatic collateral vessel is proximally embolized or is complicated by an arterial spasm during catheterization or if there is a local recurrence after chemoembolization of an extrahepatic collateral vessel, adjacent vessels can take over its territory. For example, a recurrent tumor previously supplied via the inferior phrenic artery may be supplied by the intercostal or internal mammary artery at a subsequent TACE session. It is important to catheterize extrahepatic collateral vessels by using a meticulous technique with microcatheters to prevent spasm or arterial injury and to investigate the presence or absence of collateral circulation from adjacent vessels.
In advanced stages of HCC, TACE through extrahepatic collateral arteries may not improve tumor control, because it is practically impossible to embolize multiple feeder vessels from hepatic arteries and extrahepatic collateral arteries effectively. Because omental, gastric, intercostal, renal capsular arteries supplying tumors usually develop in advanced disease, TACE through these arteries is performed less frequently.
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Conclusions
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Extrahepatic collateral vessels commonly supply HCCs if the tumors are large or peripherally located, especially along the bare area or suspensory ligaments of the liver, irrespective of the hepatic artery patency. When the presence of extrahepatic collateral vessels is suspected and the radiologist is familiar with the imaging findings, these vessels may be detected at an early stage. Chemoembolization of extrahepatic collateral vessels should be performed with a thorough knowledge of the vascular anatomy and should be performed superselectively with coaxial microcatheters to avoid possible complications.
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Footnotes
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Abbreviations: HCC = hepatocellular carcinoma, TACE = transcatheter arterial chemoembolization
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