In fact, TACE has been widely performed for patients with unresectable HCC as it was reported by Kimura et al. [11]. For HCC management via TACE approach, knowledge of the hepatic vascular supply including extrahepatic collaterals is crucial not only for understanding the strategies’ limitations but also to achieve optimal therapeutic response [12].
Sainani et al. [13] showed that hepatic tumor characterization on CT examination could be done carefully by the use of anatomical landmarks with contrast administration. Nowadays, awareness of the development of extrahepatic vascular collaterals by HCCs according either to tumor size and location or previous therapy such as surgical hepatic artery ligation or repeated chemoembolization is a prerequisite step [14].
Among these extrahepatic collaterals, the RIPA is the most common ectopic blood feeder of HCC, particularly those located at the hepatic dome [15, 22]. CT angiography with multiplanar reconstructions has become a potential non-invasive imaging technique for a variety of vascular districts. With this technique, a comprehensive quick evaluation of the RIPA anatomy can be accomplished and it can be useful in embolization planning [16].
In our study, all 58 cases were presented with hepatic dome HCC at the initial triphasic liver CT examination. According to the tumor size, the lesions were divided into three groups; < 5 cm, 5–10 cm, and ≥ 10 cm in average diameters with the corresponding cases for each group; 12 (20.7%), 39 (67.2%), and 7 (12.1%) respectively. The hepatic lesions of our cases were also divided into two groups regarding the tumor growth pattern; 23 cases (39.7%) with and 35 cases (60.3%) without liver capsule involved. The principle of involving liver capsule referred to the exophytic lesion beyond the hepatic contour. Our findings were matched with that were drawn by Sneag et al. [17].
On CT angiography, we defined ectopic tumor feeders within our cases as the vascular structures that were noticed adjacent to or penetrating the tumor. While Okino et al. [18] reported that the extrahepatic RIPA supplying HCC was suggested when the distal portion of the RIPA was observed near the liver irrespective of the relationship of the artery and tumor.
The right inferior phrenic artery usually originates from the celiac axis or directly from the aorta as a common trunk with the left inferior phrenic artery or independent origins [19]. Within our studied cases, 30 out of 33 (90.9%) with an ectopic RIP arterial supply to HCC, the RIPA has a direct origin from the abdominal aorta with only three cases (9.1%) from the celiac trunk.
Established risk factors predisposing to extrahepatic collateral arteries (ExCAs) feeding HCC include large tumors (> 5 cm), peripherally located tumors, or exophytic tumor growth should be kept under consideration when reviewing imaging or management planning [20].
To Gokan et al. [21] and Zhao et al. [22], the main reason for RIPA supply to HCC is the anatomic tumor location adjacent to the ligaments suspending the liver at the bare area. The RIPA courses on the inferior surface of the diaphragm and consequently comes in a direct contact with the hepatic dome area. Our results appreciated this finding as within our 58 cases with hepatic dome HCC, 33 cases (56.9%) were presented on CT angiography with extrahepatic collateral RIPA supply.
Our study revealed that the larger tumor size, the higher the prevalence of an extrahepatic arterial supply to HCC as 29 out of 33 cases (87.9%) with an ectopic RIPA supply were presented with a tumor size in the range of 5–10 cm, with its incidence reaching about 50% of our total 58 cases. No evidence of an ectopic blood supply to HCC smaller than 5 cm had been encountered within our cases. This was similar to the study performed by Chung et al. [12] as the probability of ExCAs in patients with a large tumor (> 5 cm) was significantly higher than that for those patients with a small tumor (< 5 cm).
Kim et al. [7] insisted that the exophytic tumor growth pattern was also a remarkable factor for the extrahepatic RIP arterial supply. As an exophytic HCC has a tendency to directly invade the diaphragm, so it can recruit a parasitic blood supply from the adjacent RIPA. In our study, 19 of 33 cases (57.6%) with extrahepatic RIPA supply, tumor displayed an exophytic component with a relatively high incidence (32.8%) within the total 58 cases. Therefore, the exophytic growth pattern of HCC was considered predictive of ExCA formation.
According to the tumor therapy, all our cases with hepatic dome HCC were managed by TACE approach. Within the total cases, 26/58 cases (44.8%) only showed a history of repeated chemoembolization. We found that 22 out of 26 cases (84.6%) with a history of repeated embolization sessions presented with extrahepatic collateral RIPA feeding HCC. This is in agreement with the studies carried out by Kim et al. [7] and kimura et al. [11] who reported that patients with repeated chemoembolization sessions usually presented by an extrahepatic collateral arterial supply to HCC even small-sized tumors as a result of attenuated lumen of the hepatic artery.
The study was performed by Sunwoo et al. [19] which widely appreciated that the extrahepatic vascular supply play a major role in tumor recurrence after receiving repeated chemoembolization. Once the number of TACE approaches has increased, the incidence of development of extrahepatic arteries has also increased as proved in our study.
In the present study, 25 out of 33 cases (75.8%) with extrahepatic RIPA supplying hepatic dome HCC were undergone embolization of both hepatic artery and extrahepatic RIPA. Follow-up triphasic liver CT examination of the previous cases revealed good prognosis with lipiodol deposition along the tumor and no evidence of residual or recurrent active lesions 3–6 months following TACE procedure. While the remaining eight cases (24.2%) with only embolized hepatic artery (HA) and non-embolized RIPA showed progressive course of the active tumor residue that supplied by the extrahepatic RIPA. So, once this extrahepatic vascular feeder was identified, the patient should underwent TACE approach via the nutrient arteries to the tumor. Our findings were consistent with the study performed by Gwon et al. [16] that observed recognition of ExCAs is crucial for effective TACE procedure.
Our 25/33 cases with embolized RIPA during TACE procedure complained of right shoulder pain with about 23/25 cases (92%) complained of hiccups. All improved gradually within a few days with conservative treatment. Minimal right pleural effusion was observed in about 17 of 25 treated cases (68%). No hemoptysis, dyspnea, or desaturation occurred. Watanabe et al. [23] showed nearly the same complications in HCC cases treated via embolization of the extrahepatic RIPA feeder. However, the previous study showed that one patient developed mild hemoptysis 4 days after TACE via the right IPA.
On the basis of our experience, the incidence of extrahepatic collateral arteries feeding HCC was positively associated with tumor size, peripheral tumor location, and the number of TACE sessions. In addition to the major vascular supply by hepatic artery, the most common EHA was the right inferior phrenic artery. This extrahepatic arterial feeder should be sought and identified in order to improve the effectiveness of TACE procedure.
We hope that this study has provided valuable information to interventionists, clinicians, and researchers alike by enhancing the understanding the anatomy of the RIPA and its potential significance in supplying hepatic dome HCC. In these cases, pre-interventional CT angiography with multiplanar reconstructions is fundamental in planning RIPA cannulation with a favorable prognosis.