Left Inferior Phrenic Artery Feeding Hepatocellular Carcinoma: Angiographic Anatomy Using C-Arm CT

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1 Vascular and Interventional Radiology Clinical Observations Kim et al. Left Inferior Phrenic rtery natomy Using C-rm CT Vascular and Interventional Radiology Clinical Observations FOCUS ON: Hyo-Cheol Kim 1 Jin Wook Chung 1 Sangbu n 1 Nak Jong Seong 1 Hwan Jun Jae 1 aik Hwan Cho 2 Jae Hyung Park 1 Kim HC, Chung JW, n S, et al. Keywords: c-arm CT, chemoembolization, hepatocellular carcinoma, left inferior phrenic artery DOI: /JR Received January 19, 2009; accepted after revision March 20, The research for this article was supported by grant from the National R & D Program for Cancer Control, Ministry of Health and Welfare, Korea. 1 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, , Korea. ddress correspondence to J. W. Chung (chungjw@snu.ac.kr). 2 Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Korea. WE This is a Web exclusive article. JR 2009; 193:W288 W X/09/1934 W288 merican Roentgen Ray Society Left Inferior Phrenic rtery Feeding Hepatocellular Carcinoma: ngiographic natomy Using C-rm CT OJECTIVE. The left inferior phrenic artery (LIP) is one of the common extrahepatic collateral arteries that supply hepatocellular carcinomas (HCCs). The purpose of this study is to describe the anatomy of the LIP that supplies HCCs using c-arm CT in 23 patients. CONCLUSION. The anteromedial limb of the ascending branch was present in 14 patients and accessory gastric branches were noted in 11 patients. The use of angiography and c-arm CT of the LIP showed 26 tumor feeders in 23 patients. The feeders were seen in the anteromedial limb (n = 12), lateral limb (n = 9), anterior limb (n = 3), and descending branch (n = 2). The anteromedial limb of the ascending branch is a common tumor feeder of the LIP and can supply HCCs located in the right liver dome. Gastric staining is also frequently depicted on LIP angiography and should not be confused with tumor staining. C hemoembolization is the most commonly used treatment method for unresectable hepatocellular carcinomas (HCCs). In practice, we frequently encounter HCCs supplied by extrahepatic collateral arteries, even when the hepatic artery is patent [1 3]. Kim et al. [1] reported that the right inferior phrenic artery is the most common extrahepatic collateral vessel that supplies HCCs, and the left inferior phrenic artery (LIP) is the sixth most common vessel that supplies HCCs. Recent flat-panel digital subtraction angiography (DS) units have used 3D rotational c-arm CT scans that are reconstructed by the use of soft-tissue windows, providing CT-like images. Several studies have shown the usefulness of c-arm CT during chemoembolization by the ability to provide additional information about vascular anatomy and tumor detection [4, 5]. lthough descriptions of the inferior phrenic artery in anatomy textbooks have been typically very brief and lacking in detail, a recent report has provided detailed anatomy of both inferior phrenic arteries [6]. However, according to our experience, the anatomy of the LIP is somewhat different from that described in the anatomic study [6]. Thus, we performed this study to describe the anatomy of the LIP that supplies HCCs using c-arm CT. Materials and Methods Patients From January 2008 to November 2008, c-arm CT of the LIP was performed in 23 patients with HCCs that had a blood supply from the LIP. The patient population consisted of 20 men and three women (age range, years; mean age, 56 years). Exclusion criteria were the following: patients who received previous embolization of the LIP, patients who had no tumor staining on LIP angiography, and patients who could not maintain breath-hold during the c-arm CT procedure. Our institutional review board approved this study, and patient informed consent was waived due to the retrospective nature of the study. diagnosis of HCC was determined on the basis of results of a percutaneous needle biopsy (n = 3), surgical resection (n = 4), or laboratory testing (i.e., the determination of an elevated serum α-fetoprotein level) in combination with typical CT and angiographic appearances and disease progression as depicted on follow-up images (n = 16). Imaging System ll 23 patients underwent contrast-enhanced multiphasic CT 1 3 weeks before chemoembolization. CT examinations were performed using various MDCT scanners that included an 8-MDCT scanner (LightSpeed Ultra, GE Healthcare) (n = 8), a 16-MDCT scanner (Sensation 16, Siemens Healthcare) (n = 6), and a 64-MDCT scanner W288 JR:193, October 2009

2 Left Inferior Phrenic rtery natomy Using C-rm CT (rilliance 64, Philips Healthcare) (n = 9). The respective scanning parameters used for the 8-, 16-, and 64-MDCT scanners were the following: detector configurations, , , and mm; slice thicknesses, 2.5, 3, and 3 mm; reconstruction intervals, 2.5, 3, and 2 mm; table speed, 13.5, 24, and 46 mm/rotation. The study was performed in an interventional procedure room equipped with a commercially available DS unit (xiom rtis dt/v30, Siemens Healthcare). One interventional radiologist with 3 years of experience in clinical practice performed all angiographic examinations. In our institution, celiac angiography, right hepatic angiography, and left hepatic angiography are routinely performed in all patients. Superior mesenteric angiography is performed at initial chemoembolization. ngiography for extrahepatic collateral vessels is performed whenever we suspect the presence of extrahepatic collateral vessel supplying a tumor on CT and celiac angiography. When selective catheterization had been achieved by placing a microcatheter with a 2.4-French tip (Microferret, Cook) or 2.0-French tip (Progreat, Terumo) as close as possible to the specific branch or branches supplying a tumor, iodized oil (Lipiodol, Guerbet), and doxorubicin hydrochloride (driamycin RDF, Ildong Pharmaceutical) emulsion was infused until stasis was achieved. If initial blockade of the feeding artery was insufficient because of large mass size or arterioportal shunting, embolization was performed using absorbable gelatin sponge particles (Gelfoam, Upjohn) 1 mm in diameter soaked in a mixture of 2 mg of crystalline mitomycin (Mitomycin-10, Kyowa Hakko Kogyo) and 10 ml of nonionic contrast medium. 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. fter we advanced the microcatheter in the proximal portion of the LIP, a single series of 3D rotational c-arm angiographic images of the LIP was obtained during a breath-hold, with 211 of circular trajectory for 8 seconds. With the use of a power injector, contrast medium (Pamiray 300, Dongkook Pharmaceutical) was injected at a flow rate of 1 2 ml/s for 12 seconds with 4 seconds of x-ray delay. The parameters for c-arm CT were as follows: 0.5 increment, matrix in projections, 211 total angle and approximately 26 per second, a system dose of approximately 0.36 µgy per frame, and 419 projections. cquired images were transferred to a commercially available dedicated workstation (Leonardo with DynaCT, Siemens Healthcare), where the 3D CT-like images were reconstructed within 1 minute. Data nalysis Two interventional radiologists with 16 years of experience in clinical practice reviewed the CT scans, conventional angiograms, and c-arm CT images to record by consensus the vascular anatomy of the LIP, the origin of the LIP, tumor staining, and the presence of tumor feeders. Tumor size was defined as the largest tumor diameter determined on transverse CT scans. Tumors were classified as single, multiple, or diffuse types in terms of multiplicity. Tumors were assigned to liver segments in accord with the Couinaud classification [7]. If a tumor occupied two or more segments, its segmental location was assigned to the dominant segment. The transverse location of a tumor was either classified to the right or left side according to the relationship between the tumor center and body midline. The proportion of blood supplied by the LIP was classified as an exclusive supply (100% of tumor staining supplied by the LIP), a dominant supply (above 50%), and a minimal supply (below 50%). The presence of tumor feeders depicted on CT was also determined by consensus. When a vessel structure was observed adjacent to or penetrating a tumor depicted on hepatic arterial phase CT and the vessel was identified as a tributary of the LIP, we considered the tumor feeder present, determined from the CT images. The branches of the LIP were classified as the ascending branch, descending branch, anterior limb of the ascending branch, lateral limb of the ascending branch, anteromedial limb of the ascending branch, adrenal branch, esophageal branch, accessory gastric branch, and accessory splenic branch [6] (Figs. 1 and 2). The anteromedial limb of the ascending branch, which has not been typically described in anatomy textbooks, was defined as a branch that originates from an ascending branch, courses below the anterior diaphragm, traverses the body midline, and supplies the anterior part of the right liver dome. The criteria for identifying the accessory gastric branch, accessory splenic branch, adrenal branch, and esophageal branch was the presence of enhancement of the stomach, spleen, adrenal gland, and esophagus, respectively, on c-arm CT. Results Tumor sizes ranged from 1.1 to 14 cm (mean, 5.2 cm). Tumor multiplicity was of the single nodular (n = 2), multinodular (n = 15), or diffuse (n = 6) type. Tumors supplied by the LIP were located as follows: segment II (n = 13), segment IV (n = 9), and segment VIII (n = 1). The transverse location of tumors supplied by the LIP was the right side (n = 11) or left side (n = 12). Left inferior phrenic arteriography was performed during the first to the 14th (mean, 5.2; median, 4) chemoembolization session. It was performed during the first session in four (17%) patients and during a repeated session in 19 (83%) patients. The LIP originated from the aorta (n = 13), celiac trunk (n = 8), left gastric artery (n = 1), and right inferior phrenic artery (RIP) (n = 1). Hepatic artery attenuation was noted in 12 patients. The proportion of the blood supply from the LIP was exclusive (n = 5), dominant (n = 9), or minimal (n = 9). We have not experienced Fig. 1 Schematic diagram shows typical configuration of left inferior phrenic artery: 1 = ascending branch, 2 = descending branch, 3 = anterior limb, 4 = lateral limb, 5 = anteromedial limb, 6 = accessory gastric branch, and 7 = adrenal branch. JR:193, October 2009 W289

3 Kim et al. any complications of chemoembolization in this study population. scending branches were seen in all 23 patients (Figs. 3 5), but the descending branches were not seen in five patients (Fig. 3). The common trunk of the descending and ascending branches was noted in 16 of 18 patients who had descending branches. In the remaining two patients, the descending branch arose from the celiac trunk in one patient whose LIP originated from the left gastric artery and from the aorta in another patient whose LIP originated from the RIP (Fig. 5). drenal branches were seen in all 23 patients, but accessory gastric branches were present in 11 patients (Figs. 3 and 4). The esophageal branch and accessory splenic branch were present in only one patient, respectively. The anteromedial limb of the ascending branch was present in 14 patients (Fig. 3). ngiography and c-arm CT of the LIP showed the presence of 26 tumor feeders in 23 patients. The feeders were located in the anteromedial limb (n = 12), lateral limb (n = 9), anterior limb (n = 3), and descending branch (n = 2). CT scans showed the presence of 10 tumor feeders located in the anteromedial limb (n = 6) (Fig. 3), lateral limb (n = 3), and anterior limb (n = 1). On CT scans, the anteromedial limb of the ascending branch was noted in 13 patients. In six of the 13 patients, the anteromedial limb reached the tumor seen on a CT scan, which Fig year-old man with hepatocellular carcinoma treated with nine sessions of chemoembolization., CT scan shows small hypervascular mass (arrow) in right liver dome. nteromedial branch (arrowheads) of left inferior phrenic artery was seen on CT scan. Hepatic arteriography showed no tumor staining (not shown)., Inferior phrenic arteriogram at 10th session of chemoembolization shows tumor staining (black arrow) supplied by anteromedial limb (black arrowheads) of ascending branch of left inferior phrenic artery. Note accessory gastric branch (white arrow), gastric staining (open white arrowhead), anterior limb (open black arrowhead), lateral limb (open black arrow), and descending branch (open white arrow). Left inferior phrenic artery arises from common trunk of right inferior phrenic artery. Contrast medium was refluxed into left subcostal artery (white arrowhead). was interpreted as a tumor feeder, and angiography confirmed that the anteromedial limbs were tumor feeders in the six patients. In the remaining seven patients, the proximal portion of the anteromedial limb was noted on a CT scan, but it did not reach the tumor seen on a CT scan and was not interpreted as a tumor feeder. However, angiography showed that the anteromedial limbs were tumor feeders in six of seven patients. Table 1 shows the angiographic findings for all patients. Discussion We found that the anteromedial limb is the most common tumor feeder of the LIP. lthough anatomy textbooks and reports have not provided information concerning this branch, Suh et al. [8] have shown the presence of this anteromedial limb on angiographic images. The presence of the anteromedial limb indicates that the LIP can supply the tumors in the right liver dome. Ohashi et al. [9] reported the top of the liver under the right side of the diaphragm consisted of the right lobe (segments VII and VIII) in 41% of individuals, both lobes (segments IV and VIII) in 54%, and only the left lobe (segments II and IV) in 5%. In our study, 11 (48%) tumors were in the right side of body. In addition, the anteromedial limb frequently can be observed on MDCT scans if it is present. When a tumor is present in the right liver dome and a prominent anteromedial limb is seen on a CT scan, angiography of the LIP should be performed. It is known that a tumor in the right liver dome can be supplied by the hepatic, right inferior phrenic, or right internal mammary arteries [1, 10, 11], and the LIP may also supply a tumor in the right liver dome. We think that the LIP may supply subcapsular lesions in segments II IV and occasionally segment VIII of the liver, and the right inferior phrenic artery could supply lesions in segments VII and VIII and occasionally segment IV. In our study, accessory gastric branches were present in 11 (48%) patients. However, the previous anatomic study omitted the accessory gastric branches [6]. In addition, there have been reports of gastroesophageal hemorrhage due to bleeding from the LIP [12] and of gastric toxicity related to perfusion of the stomach via the LIP during hepatic arterial infusion chemotherapy [13]. ccessory gastric branches of the LIP supplying gastric staining can be observed in one half of patients and should not be confused with tumor staining. ecause the accessory gastric branches show a typical corkscrew appearance around gastric staining, it is not difficult to perceive gastric staining in most cases [14, 15]. In some cases, however, it is important to obtain delayed angiographic images that show draining of the gastric vein to discriminate gastric staining from tumor staining. W290 JR:193, October 2009

4 Left Inferior Phrenic rtery natomy Using C-rm CT E C Fig year-old man with hepatocellular carcinoma., Serial CT scans show large hypervascular mass (M) in right liver dome. Hepatic arteriography showed huge tumor staining, but right inferior phrenic arteriography showed no tumor staining (not shown). Note ascending branch (arrowhead), bifurcation of anterior limb and anteromedial limb (open arrow), and anteromedial limb (solid arrows) of left inferior phrenic artery., Left inferior phrenic arteriogram at initial session of chemoembolization shows tumor staining (M) supplied by anteromedial limb (solid arrows) of ascending branch. There is no descending branch. Note gastric staining (star), adrenal gland staining (open arrowhead), anterior limb (open arrow), and lateral limb (solid arrowhead). C, Contrast-enhanced c-arm CT images show tumor staining (solid arrowheads) supplied by anteromedial limb (solid arrows). Note enhancement of gastric cardia (open arrowheads) and distal esophagus (open arrow). D, Superior volume rendering image of c-arm CT with 65 craniocaudal angle shows tumor staining (solid arrowheads) supplied by anteromedial limb (solid arrow). Note anterior limb (open arrow) and lateral limb (open arrowhead). E, Spot image obtained after embolization through anteromedial branch of left inferior phrenic artery. Note iodized oil uptake in tumor (arrowheads) and tip (arrow) of microcatheter. D JR:193, October 2009 W291

5 Kim et al. The nomenclature of branches of the phrenic artery varies according to different published reports. In our study, the dividing branches of the LIP were denoted as the ascending and descending branches, but some reports refer to these branches as medial and lateral or anterior and posterior, respectively [6, 16]. The descending branches were not seen on angiography in five of 23 patients. There is a possibility that the descending branches separately arise from the aorta, celiac trunk, or left renal artery, and Fig year-old man with hepatocellular carcinoma., CT scan shows large hypervascular mass (arrows) in left liver dome., Left inferior phrenic arteriogram at initial session of chemoembolization shows tumor staining (star) supplied by anterior limb (open arrowhead) and lateral limb (black arrowhead) of ascending branch and descending branch (open arrow). Note gastric staining (white arrowheads) supplied by accessory gastric branch (solid arrow). we were unable to visualize the descending branches with angiography. ccording to a recent anatomic study of 300 cases [6], the origins of the LIP were from the celiac trunk (47%), aorta (45%), renal artery (5%), left gastric artery (2%), and hepatic artery proper (1%). In another study of 140 cases of right inferior phrenic angiography [16], there were 20 cases (14.3%) in which the ascending branch of the LIP arose from the RIP, which has not been described in anatomic studies [6]. In our study, one patient showed the ascending branch originating from the RIP and the descending branch arising from the aorta. The differences may be attributed to a high degree of variability. Okino and colleagues [17] insisted that visualization of the RIP at the distal portion on a single-detector CT scan would be a clue for a parasitic supply from the RIP, and it was evident in 75% of patients that had tumors fed by the RIP. In our study, tumor feeders were visualized on a CT scan in only Fig year-old man with hepatocellular carcinoma treated with two sessions of chemoembolization., CT scan shows hypovascular tumor (solid arrowheads) in segment II. Note previously infused iodized oil (arrow) and dilated left inferior phrenic artery (open arrowhead)., Right inferior phrenic arteriogram at third session of chemoembolization shows ascending branch (solid arrow) of left inferior phrenic artery arising from right inferior phrenic artery. Note tumor staining (white arrowheads) supplied by ascending branch and systemic-to-pulmonary shunt (black arrowhead) mainly supplied by lateral limb (open arrowhead). Note descending branch (open arrow) arising from aorta. W292 JR:193, October 2009

6 Left Inferior Phrenic rtery natomy Using C-rm CT TLE 1: Summary of ngiographic Findings of Left Inferior Phrenic rtery (LIP) Supplying Hepatocellular Carcinoma Patient No. Sex ge (y) No. of Previous TCE Sessions Tumor Size (mm) Tumors Supplied by LIP (Segment) Transverse Location Origin of LIP ccessory Gastric ranch nteromedial Limb Tumor Feeder History of RIP Embolization 1 M IV Right orta bsent Present nteromedial limb No 2 M IV Right orta Present Present nteromedial limb No 3 F II Left orta bsent bsent Lateral limb Yes 4 M IV Right orta Present Present nteromedial limb No 5 M II Left orta bsent bsent Lateral limb No 6 M II Left orta bsent bsent Lateral limb No 7 M II Left orta Present Present Lateral limb Yes 8 M IV Right orta Present Present nteromedial limb Yes 9 M II Left orta Present Present nteromedial limb, anterior limb Yes 10 M IV Right orta Present Present nteromedial limb Yes 11 M IV Right orta bsent Present nteromedial limb Yes 12 M II Left orta bsent Present Lateral limb, descending branch No 13 M II Left orta Present bsent Lateral limb Yes 14 F II Left Celiac Present bsent Lateral limb, descending branch No 15 M IV Right Celiac bsent Present nteromedial limb No 16 M II Left Celiac bsent bsent Lateral limb No 17 M II Left Celiac bsent bsent Lateral limb Yes 18 F IV Right Celiac Present Present nteromedial limb No 19 M II Right Celiac Present Present nteromedial limb No 20 M II Left Celiac Present bsent nterior limb Yes 21 M VIII Right Celiac bsent Present nteromedial limb No 22 M IV Right LG N Present nteromedial limb No 23 M II Left RIP bsent bsent nterior limb No Note TCE = transarterial chemoembolization, RIP = right inferior phrenic artery, LG = left gastric artery, N = not applicable. 10 (43%) patients who had tumors fed by the LIP, despite the use of MDCT with a thin slice thickness. We recently reported that tumor feeders were visualized on MDCT scans in only 56% of patients who had tumors fed by the RIP [18]. We defined tumor feeders as vessel structures that were observed adjacent to or penetrating a tumor. In the study by Okino et al., the distal portion of the RIP was noted irrespective of the relationship of the vessel and tumor. In our study, the anteromedial limb was noted on MDCT in 13 patients and was considered as a tumor feeder in six at MDCT. However, the anteromedial limb was proven to be a tumor feeder in 12 of 13 patients at angiography and c-arm CT. We think that angiography of the LIP is mandatory when the anteromedial limb is evident on a CT scan and viable tumor is present in the right liver dome. There are some limitations to our study. First, the study population was small because we included patients with HCCs supplied by the LIP. Second, we did not study the vascular anatomy of the LIP in patients who had HCCs without a blood supply from the LIP. We think that the prevalence of the anteromedial limb might be lower in the normal population because patients who had the anteromedial limb had a large vascular territory of the diaphragm and had a high probability of having a collateral blood supply to tumors from the LIP. In addition, because patients in our study had a mean of 5.2 sessions of chemoembolization, it is possible that the presence of liver tumor and previous chemoembolization may have activated collateral or silent circulation of the LIP. Third, c-arm CT has a limited field of view [19], and terminal branches of the LIP were not included in the c-arm CT images in several patients. In conclusion, our findings indicate that the use of c-arm CT of the LIP can provide detailed vascular anatomy and an exact discrimination between tumor staining and nontumor staining. The anteromedial limb of the ascending branch is one of the common tumor feeders of the LIP and can supply HCCs located in the right liver dome. Gastric staining is also frequently observed with the use of LIP angiography and should not be confused with tumor staining. References 1. Kim HC, Chung JW, Lee W, Jae HJ, Park JH. Recognizing extrahepatic collateral vessels that supply hepatocellular carcinoma to avoid complications of transcatheter arterial chemoembolization. RadioGraphics 2005; 25[suppl 1]:S25 S39 2. Chung JW, Kim HC, Yoon JH, et al. Transcatheter arterial chemoembolization of hepatocellular carcinoma: prevalence and causative factors of extrahepatic collateral arteries in 479 patients. Korean J Radiol 2006; 7: Miyayama S, Matsui O, Taki K, et al. Extrahepatic JR:193, October 2009 W293

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