Published online before print January 17, 2007, 10.1148/radiol.2423060220
(Radiology 2007;242:925-932.)
© RSNA, 2007
Vascular and Interventional Radiology |
Internal Mammary Arteries Supplying Hepatocellular Carcinoma: Vascular Anatomy at Digital Subtraction Angiography in 97 Patients1
Hyo-Cheol Kim, MD,
Jin Wook Chung, MD,
Seung Hong Choi, MD,
Hwan Jun Jae, MD,
Whal Lee, MD and
Jae Hyung Park, MD
1 From the Department of Radiology, Seoul National University College of Medicine; 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. Received February 5, 2006; revision requested April 3; revision received April 6; accepted May 10; final version accepted July 10.
Address correspondence to J.W.C. (e-mail: chungjw{at}radcom.snu.ac.kr).
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ABSTRACT
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Purpose: To retrospectively evaluate the vascular anatomy of the internal mammary arteries that supply hepatocellular carcinomas (HCCs), with an emphasis on number of tumor feeders.
Materials and Methods: This retrospective study was approved by the institutional review board; informed consent was waived. Between August 1996 and July 2005, internal mammary arteries that supply HCCs were found in 97 (2.2%) of 4438 patients (76 men, 21 women; mean age, 55 years ± 10.5 [standard deviation]; range, 19–79 years). Computed tomographic scans and digital subtraction angiograms in these 97 patients were retrospectively reviewed in consensus by two interventional radiologists. Tumor size, number of tumor feeders, and tumor location were recorded. The t test and analysis of variance were used to correlate tumor size with number of tumor feeders, tumor feeder laterality, and transcatheter arterial chemoembolization (TACE) time.
Results: The following 125 tumor feeders were identified in 97 patients: phrenic branch (n = 59), musculophrenic artery (n = 40), superior epigastric artery (n = 15), anterior intercostal artery (n = 6), ensiform artery (n = 4), and pericardiacophrenic artery (n = 1). In two patients, tumors were in dorsal hepatic areas directly beneath the diaphragm. Half of the tumors located in liver segments II or III were supplied by the right internal mammary artery. In three patients, the tumor feeders from the left internal mammary artery crossed the midline. Tumor size was not statistically associated with number of tumor feeders (P = .076), tumor feeder laterality (P = .141), and TACE time (P = .729).
Conclusion: The common tumor feeders of the internal mammary artery are the phrenic branch and the musculophrenic artery. Moreover, the internal mammary artery can supply a tumor even in the dorsal hepatic area.
© RSNA, 2007
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INTRODUCTION
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Transcatheter arterial chemoembolization (TACE) is widely used in the management of hepatocellular carcinoma (HCC) (1,2). 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 exclusively supplied by the hepatic artery. In clinical practice, however, we frequently encounter HCCs supplied by extrahepatic collateral arteries (eg, the inferior phrenic artery, adrenal artery, intercostal artery, internal mammary artery, and the omental branch) even when the hepatic artery is widely patent (3–12).
Nakai et al (13) have noted that, regardless of tumor size, when HCCs are located in the ventral hepatic area directly beneath the diaphragm, the internal mammary artery can serve as a feeding artery in patients with hepatic artery occlusion caused by repeated TACE. Cutaneous complications of TACE performed through the internal mammary artery have been reported and are similar to skin injuries caused by the extravasation of chemotherapeutic drugs (14,15). Thus, in patients who undergo TACE through extrahepatic collateral vessels, the procedure should be performed with a thorough knowledge of the vascular anatomy. The purpose of this study, therefore, was to retrospectively evaluate the vascular anatomy of the internal mammary arteries that supply HCCs, with an emphasis on the number of tumor feeders.
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MATERIALS AND METHODS
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This retrospective study was approved by our institutional review board; informed consent was waived.
Patients
From August 1996 to July 2005, 15 295 sessions of TACE were performed in 4438 patients with HCC at our institution. In 97 (2.2%) of these 4438 patients, we found an internal mammary artery that supplied the HCC. These patients included 76 men and 21 women with ages ranging from 19 to 79 years (mean, 55 years ± 10.5 [standard deviation]). A diagnosis of HCC was rendered on the basis of the results of percutaneous needle biopsy (n = 6), surgical resection (n = 22), or clinical or laboratory testing (eg, elevated serum 
-fetoprotein levels and viral markers) in combination with typical computed tomographic (CT) and digital subtraction angiographic (DSA) appearances and disease progression on follow-up images (n = 69). Six patients had undergone percutaneous ethanol injection.
Methods of Chemoembolization
In all patients, enhanced biphasic helical CT scans of the liver were obtained before TACE was performed. Various single-detector (n = 61) or multidetector (n = 36) CT scanners with variable section thickness were used. CT parameters for single-detector scanners were the following: collimation, 7–10 mm; table pitch, 1:1; and reconstruction interval, 7–10 mm. CT parameters for multidetector scanners were the following: detector collimation, 1.25–2.5 mm; table speed, 15–25 mm per rotation; gantry rotation, 0.5–0.75 second; section thickness, 2.5–5 mm. The section thickness was 2.5 or 3.2 mm in 29 patients and 5 mm or more in 68 patients.
All DSA examinations were performed by one of two interventional radiologists (J.W.C., with 14 years of experience, or J.H.P., with 25 years of experience at the end of the study in 2005). Selective DSA of the internal mammary artery by using a 5-F catheter (DAV; Cook, Bloomington, Ind) was performed to detect tumor staining in the following instances: first, when an HCC was located in the ventral hepatic area and tumor staining on a hepatic angiogram had a focal defect; second, when iodized oil that was infused at a previous TACE session had not accumulated in the ventral portion of the tumor on a CT scan; and third, when a viable tumor that abutted the diaphragm was located in the dorsal hepatic portion on a CT scan and its correspondent tumor staining was not observed by using hepatic and inferior phrenic angiography. We selectively chose the right or left internal mammary artery on the basis of the CT findings. If ipsilateral internal mammary artery DSA failed to reveal tumor staining, contralateral internal mammary artery DSA was performed.
When superselective catheterization was achieved by placing a 2.4- or 3-F microcatheter (Microferret; Cook) tip as close as possible to a specific branch or to branches that supplied tumor staining, we infused iodized oil (Lipiodol; Andre Gurbet, Aulnay-sous-Bois, France) and doxorubicin hydrochloride (Adriamycin RDF; Ildong Pharmaceutical, Seoul, Korea) emulsion until stasis was achieved. An emulsion of 0.4–5 mL of iodized oil and 2–30 mg of doxorubicin hydrochloride was infused through the internal mammary artery according to tumor size. We infused the chemotherapeutic agent (up to 12 mL of iodized oil and 60 mg of doxorubicin hydrochloride) through the hepatic artery and all extrahepatic collateral arteries in one session. A spot image was obtained during infusion to verify microcatheter tip location. Contrast agent (Ultravist; Schering Korea, Seoul, Korea) was injected during 6–8 seconds with a flow rate of 2–3 mL/sec for a 5-F catheter and a flow rate of 0.7–1.5 mL/sec for a 2.4- or 3-F microcatheter.
Data Analysis
Data were recorded in an electronic database (Access; Microsoft, Redmond, Wash) immediately following DSA by one of two individuals (J.W.C. or J.H.P.). These data included the date of the procedure, the number of previous TACE sessions, the amounts of iodized oil and anticancer agents used, the artery into which the iodized oil and anticancer agents were infused, the presence of an extrahepatic collateral artery that supplied a tumor, anatomic descriptions of the hepatic and extrahepatic collateral arteries, the presence of stenosis or occlusion of the hepatic artery, and the presence of complications (eg, skin rash).
CT scans and DSA images in these 97 patients were retrospectively reviewed in consensus by two interventional radiologists who had performed all TACE procedures. Tumor feeders were classified as the pericardiacophrenic artery, musculophrenic artery, superior epigastric artery, anterior intercostal artery, or ensiform artery or as the phrenic branch (Fig 1) (16–19). The phrenic branch, which passes through anterior pericardial fat, was also divided into high (third or higher intercostal space) or low (fourth or lower intercostal space) types according to its level of origin. In 29 patients in whom repeated TACE was performed through the internal mammary artery, we included only the tumor feeder that was observed at the TACE session in which the internal mammary artery that fed a tumor was first detected.
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Figure 1: Schematic diagram of the internal mammary artery. 1 = Pericardiacophrenic artery, 2 = superior epigastric artery, 3 = musculophrenic artery, 4 = diaphragmatic branch of musculophrenic artery, 5 = anterior intercostal artery, 6 = phrenic branch, 7 = ensiform artery.
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Tumor size was defined as the largest tumor diameter on transverse CT scans. Tumors were assigned to liver segments in accordance with the Couinaud classification (20). If a tumor occupied two or more segments, the location of the tumor was assigned to the dominant segment. A positional tumor location was classified as anterior or posterior. When a tumor was in contact with the anterior half of the diaphragm on a transverse CT scan, the location was assigned as anterior; when a tumor was in contact with only the posterior half of the diaphragm, the location was considered posterior. In consensus, we also recorded whether the tumor feeder was depicted on a CT scan.
Statistical Analysis
We performed the t test to determine tumor size differences between two groups (patients receiving initial TACE vs patients receiving repeated TACE and tumors fed by a single tumor feeder vs tumors fed by multiple tumor feeders) and analysis of variance with Tukey post hoc comparisons among three groups (right vs left vs both internal mammary arteries as tumor feeders). Differences with P < .05 were considered statistically significant. Data processing and analysis were performed by using software (SPSS, version 10.0; SPSS, Chicago, Ill).
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RESULTS
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Tumor sizes ranged from 1.5 to 20 cm (mean, 8.25 cm). Tumors were located as follows: liver segment IV (n = 54), liver segment VIII (n = 12), liver segments II and III (n = 24), liver segment VII (n = 1), pericardial lymph node (n = 3), abdominal wall metastasis (n = 2), and diaphragmatic metastasis (n = 1). All hepatic tumors abutted the liver surface or the diaphragm. A positional tumor location was classified as anterior (n = 95) or posterior (n = 2). Involvement of the internal mammary artery was detected at TACE sessions 1–26 (mean, 5.4 sessions; median, 4 sessions); involvement of this artery was detected at the initial session in 16 (16%) of 97 patients and at the repeated session in 81 (84%) of them. Time from performance of initial TACE to performance of internal mammary artery DSA ranged from 0 to 162 months (mean, 23.8 months; median, 10 months). In 72 (74%) patients, the hepatic artery was widely patent when the DSA image of the internal mammary artery was obtained. In six (6%) patients, the right hepatic (n = 3) or left hepatic (n = 3) artery was occluded by using repeated TACE. In 19 (20%) patients, severe stenosis or occlusion of the segmental hepatic artery was noted when the DSA image of the internal mammary artery was obtained.
Tumor Supply and Tumor Feeders
Tumors were supplied by the right internal mammary artery (n = 79), the left internal mammary artery (n = 12), or both (n = 6) (Table 1) (Figs 2–6). The numbers of tumor feeders per patient were one (n = 71), two (n = 24), and three (n = 2). The 59 phrenic branches were classified as either the high (n = 3) or the low (n = 56) type (Figs 2, 3).
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Figure 2a: HCC supplied by the phrenic branch (high origin) of left internal mammary artery in a 41-year-old man. (a) Posteroanterior DSA image of internal mammary artery shows phrenic branch of high origin (solid arrowheads) and musculophrenic artery (arrow) supplying tumor staining. Note lateral costal branch (open arrowhead). (b) Lateral DSA image of internal mammary artery shows phrenic branch of high origin (arrowheads) and musculophrenic artery (arrow) that supply tumor staining. Note the course of the phrenic branch through the anterior mediastinum.
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Figure 2b: HCC supplied by the phrenic branch (high origin) of left internal mammary artery in a 41-year-old man. (a) Posteroanterior DSA image of internal mammary artery shows phrenic branch of high origin (solid arrowheads) and musculophrenic artery (arrow) supplying tumor staining. Note lateral costal branch (open arrowhead). (b) Lateral DSA image of internal mammary artery shows phrenic branch of high origin (arrowheads) and musculophrenic artery (arrow) that supply tumor staining. Note the course of the phrenic branch through the anterior mediastinum.
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Figure 3a: Recurrent tumor supplied by the phrenic branch (low origin) of the right internal mammary artery in a 40-year-old man who underwent right lobectomy. (a) Transverse CT scan in portal venous phase shows low-attenuating nodule (arrowheads). (b) Posteroanterior DSA image of internal mammary artery shows tumor staining (arrowhead) supplied by the phrenic branch of low origin (arrow).
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Figure 3b: Recurrent tumor supplied by the phrenic branch (low origin) of the right internal mammary artery in a 40-year-old man who underwent right lobectomy. (a) Transverse CT scan in portal venous phase shows low-attenuating nodule (arrowheads). (b) Posteroanterior DSA image of internal mammary artery shows tumor staining (arrowhead) supplied by the phrenic branch of low origin (arrow).
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Figure 4a: HCC supplied by the musculophrenic artery of the right internal mammary artery in a 45-year-old man. (a) Transverse CT scan shows multiple enhancing tumors (T) in liver. (b) Posteroanterior DSA image of internal mammary artery shows tumor staining supplied by the hypertrophied diaphragmatic branches (solid arrowheads) of the musculophrenic artery. Note phrenic branch (open arrowhead).
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Figure 4b: HCC supplied by the musculophrenic artery of the right internal mammary artery in a 45-year-old man. (a) Transverse CT scan shows multiple enhancing tumors (T) in liver. (b) Posteroanterior DSA image of internal mammary artery shows tumor staining supplied by the hypertrophied diaphragmatic branches (solid arrowheads) of the musculophrenic artery. Note phrenic branch (open arrowhead).
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Figure 5: HCC supplied by the superior epigastric artery of right internal mammary artery in a 59-year-old man. Posteroanterior DSA image of internal mammary artery shows tumor staining (arrowheads) supplied by the hypertrophied superior epigastric artery (arrow).
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Figure 6: HCC supplied by the ensiform artery of right internal mammary artery in a 55-year-old man. Posteroanterior DSA image of internal mammary artery shows tumor staining supplied by the ensiform artery (arrowhead). Note faintly visualized branches (arrows) of left hepatic artery.
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Tumors located in liver segment II or III were fed by the left internal mammary artery (n = 12), the right internal mammary artery (n = 11), or both (n = 3) (Table 2). Although tumors located in liver segment IV were most commonly supplied by the right phrenic branch, tumors in liver segment VIII were most commonly supplied by the right musculophrenic artery. Two tumors with a posterior location were supplied by a tumor feeder from the anterior intercostal artery (Fig 7) or the musculophrenic artery. The two patients with these tumors had undergone TACE through the right inferior phrenic artery prior to chemoembolization through the internal mammary artery. In three patients, tumor feeders from the left internal mammary artery crossed the midline to supply tumors (Fig 2).
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Table 2. Relationship between Tumor Feeder and Tumor Location in Patients with HCC Supplied by Internal Mammary Artery
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Figure 7a: HCC supplied by the anterior intercostal artery of right internal mammary artery in a 63-year-old man. (a) Transverse CT scan shows enhancing nodule (arrow) in liver segment VIII. DSA images of hepatic artery and right inferior phrenic artery showed no tumor staining (not shown). (b) Posteroanterior DSA image of internal mammary artery shows tumor staining supplied by the diaphragmatic branches (solid arrowheads) of the anterior intercostal artery (curved arrow) arising from the musculophrenic artery (straight arrow). Note phrenic branch (open arrowhead). (c) Spot image obtained during chemoembolization shows compact uptake of iodized oil (arrowheads). Note the tip (arrow) of the microcatheter.
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Figure 7b: HCC supplied by the anterior intercostal artery of right internal mammary artery in a 63-year-old man. (a) Transverse CT scan shows enhancing nodule (arrow) in liver segment VIII. DSA images of hepatic artery and right inferior phrenic artery showed no tumor staining (not shown). (b) Posteroanterior DSA image of internal mammary artery shows tumor staining supplied by the diaphragmatic branches (solid arrowheads) of the anterior intercostal artery (curved arrow) arising from the musculophrenic artery (straight arrow). Note phrenic branch (open arrowhead). (c) Spot image obtained during chemoembolization shows compact uptake of iodized oil (arrowheads). Note the tip (arrow) of the microcatheter.
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Figure 7c: HCC supplied by the anterior intercostal artery of right internal mammary artery in a 63-year-old man. (a) Transverse CT scan shows enhancing nodule (arrow) in liver segment VIII. DSA images of hepatic artery and right inferior phrenic artery showed no tumor staining (not shown). (b) Posteroanterior DSA image of internal mammary artery shows tumor staining supplied by the diaphragmatic branches (solid arrowheads) of the anterior intercostal artery (curved arrow) arising from the musculophrenic artery (straight arrow). Note phrenic branch (open arrowhead). (c) Spot image obtained during chemoembolization shows compact uptake of iodized oil (arrowheads). Note the tip (arrow) of the microcatheter.
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In 75 (77%) patients, CT failed to depict the tumor feeder. In 22 (23%) patients, 25 tumor feeders were observed on CT scans; these were the phrenic branch (n = 16) and the musculophrenic (n = 7) and anterior intercostal arteries (n = 2). In 29 patients in whom a CT scan was obtained with a section thickness of 3.2 mm or smaller, tumor feeders were observed in 17 (59%).
Complications
Cutaneous complications, such as a skin rash, occurred in seven (7%) patients. The embolized vessels in these seven patients were the superior epigastric artery (n = 3), the anterior intercostal artery (n = 2), and the phrenic branch (n = 2). Seven patients with a skin rash were treated with observation, and no patient experienced skin necrosis.
Statistical Analysis
Tumor size was not significantly associated with number of tumor feeders (one vs many), tumor feeder laterality (right internal mammary artery vs left internal mammary artery vs both arteries), and TACE time (initial session vs repeated session) (Table 3).
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DISCUSSION
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The internal mammary artery usually arises from the proximal part of the subclavian artery (18,19). The lateral costal branch, which seldom supplies the diaphragm, arises above the first rib and courses laterally and downward into the lateral chest wall. The pericardiacophrenic artery usually arises above the second intercostal space and gives branches to the pleura, pericardium, and diaphragm (18,19). At the level of the sixth intercostal space, the artery divides into two end arteries, the musculophrenic and superior epigastric arteries. The musculophrenic artery courses laterally and downward, giving off the vertical diaphragmatic branches and intercostal branches to the lowest intercostal spaces, and this pattern creates a lattice appearance. The superior epigastric artery passes vertically downward and anastomoses with the inferior epigastric artery (18).
In anatomy textbooks, a pericardiacophrenic artery is described that accompanies the phrenic nerve between the pleura and the pericardium; descriptions in these textbooks state that the artery is distributed to the diaphragm (18,19). Investigators in a recent article about the anatomic structure of the pericardiacophrenic artery also reported that it originated from the internal mammary artery in 89% of 100 dissected cadavers (21). Singh (16), however, reported that a constant artery of this description was not encountered and most arteries could not be traced to the diaphragm. Thus, Singh proposed the term long pericardial branches as a more accurate description. In our study, only one patient had a tumor supplied by a pericardiacophrenic artery with a phrenic nerve course. Moreover, 96 patients had fine pericardial and/or mediastinal branches that did not reach the diaphragm. This discrepancy can be explained by the following two ideas: that the diaphragmatic twig of the pericardiacophrenic artery is so small that DSA fails to depict it or that the anatomists have overestimated diaphragmatic supply by the pericardiacophrenic artery.
We found that the phrenic branch usually arose between the fourth and sixth intercostal spaces and passed through anterior pericardial fat. Although anatomy textbooks offer no information about this branch (18,19), Singh stated that "muscular branches to the diaphragm" arose between the third and sixth intercostal spaces and were found in 20 of 100 patients (16). We found, however, that the most common tumor feeder was the phrenic branch (n = 59) in 58 (60%) of 97 patients. This discrepancy can be explained as follows: Most phrenic branches are too small to be observed by using DSA in the normal population, but when a phrenic branch supplies a tumor, then it becomes hypertrophied sufficiently to be depicted by using DSA.
We previously reported that the pericardiacophrenic artery supplies HCCs in about two-thirds of patients and that the musculophrenic artery supplies them in about one-third of patients (6). In our study, however, we discriminated between the phrenic branch and the pericardiacophrenic artery, because the phrenic branch does not course along the phrenic nerve and usually arises at a lower level of the internal mammary artery. Our study findings indicate that the phrenic branch makes up about a half of tumor feeders, that the musculophrenic artery constitutes one-third of tumor feeders, and that other tumor feeders account for the remainder of tumor feeders.
Nakai et al (13) advised that internal mammary artery DSA be performed for tumors located in ventral hepatic areas directly beneath the diaphragm. In two patients with a tumor in a posterior location, however, tumors were supplied by the internal mammary arteries. These two patients had received TACE treatment through the right inferior phrenic artery prior to chemoembolization through the internal mammary artery. We postulated that previous chemoembolization through the right inferior phrenic artery had caused the internal mammary artery to take over its territory, because terminal branches of the two arteries were observed to have anastomosis (6).
An anastomosis between the hepatic falciform artery and the internal mammary artery through the ensiform artery has been demonstrated by using cadaveric dissection (22) and angiography (23). In our study, four ensiform arteries that fed HCCs were demonstrated in three patients. The tumors supplied by ensiform arteries were anteriorly exophytic tumors in liver segment III, and these tumors were similar to those supplied by the superior epigastric artery. Although the ensiform artery courses vertically downward and supplies anterior liver segment III, the phrenic branch makes a J- or U- turn and supplies the anterosuperior diaphragm.
Nakai et al (13) found that tumors located in liver segment VIII or IV are fed by the right internal mammary artery, whereas those located in liver segment II or III are supplied by the left internal mammary artery. In our study, half of the tumors located in liver segment II or III were supplied by the right internal mammary artery, because the border between liver segment III–liver segment II and liver segment IV is not at midline but is slightly removed to the right.
In our study, a skin rash occurred in seven patients. Anterior intercostal or superior epigastric arteries were embolized in five of these seven patients; both of these arteries possess branches that feed the skin, and this finding indicates that selective embolization is needed in such cases. Skin rashes occurred in two patients in whom phrenic branches were embolized, and these were attributed to chemotherapeutic agent reflux into the main artery. Thus, selection of a tumor feeder and incremental agent injection are important considerations to prevent cutaneous complications.
Some limitations of our study should be mentioned. First, our study was not a prospective trial. In our database, moreover, we did not record the negative results of internal mammary artery DSA. Thus, predictors of internal mammary supply on a CT scan and influential factors in formation of collateral blood supply could not be evaluated. Second, we performed internal mammary artery DSA in patients who were suspected of having a blood supply to a tumor. We may have missed unsuspected arterial feeders from the internal mammary artery in some patients. In our clinical practice, internal mammary artery DSA was not performed in some patients who had HCC at an advanced stage despite a suspicion of a collateral blood supply. Thus, the frequency of 2.2% for an internal mammary artery supply may be somewhat underestimated. Third, various single- or multidetector CT scanners were used with variable parameters in our study.
In conclusion, although the pericardiacophrenic artery seldom supplies an HCC, the common tumor feeders from the internal mammary artery are the phrenic branch and the musculophrenic artery. Uncommonly, the internal mammary artery can supply a tumor even in dorsal hepatic areas directly beneath the diaphragm.
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ADVANCES IN KNOWLEDGE
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- The common tumor feeders from the internal mammary artery are the phrenic branch and the musculophrenic artery.
- The pericardiacophrenic artery seldom supplies a hepatocellular carcinoma (HCC).
- The internal mammary artery can supply tumors that are in dorsal hepatic areas directly beneath the diaphragm.
- Half of the tumors located in liver segment II or III were supplied by the right internal mammary artery.
- Tumor feeders from the internal mammary artery can infrequently cross the midline to supply the HCC.
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FOOTNOTES
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Abbreviations: DSA = digital subtraction angiography • HCC = hepatocellular carcinoma • TACE = transcatheter arterial chemoembolization
Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, J.W.C.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, all authors; clinical studies, all authors; statistical analysis, H.C.K., H.J.J.; and manuscript editing, all authors
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ABSTRACT
INTRODUCTION
