Volume 20, Issue 7 , Pages 888-895, July 2009
Transcatheter Arterial Chemoembolization for Hepatocellular Carcinoma: Prospective Assessment of the Right Inferior Phrenic Artery with C-arm CT
Article Outline
Purpose
To assess the usefulness of C-arm computed tomography (CT) of the right inferior phrenic artery (RIPA) in transcatheter arterial chemoembolization of patients with hepatocellular carcinoma (HCC).
Materials and Methods
From December 2007 to April 2008, C-arm CT of the RIPA was prospectively performed in 32 patients with HCC. Two interventional radiologists who performed C-arm CT assessed the additional information provided with C-arm CT as grade 1 (no additional information), grade 2 (added information without an effect on the treatment plan), or grade 3 (added information with an effect on the treatment plan). Tumor feeders and feeders of a systemic-to-pulmonary shunt were recorded.
Results
The information provided by C-arm CT was classified as grade 1 for nine of the 32 patients (28%), grade 2 for 20 patients (63%), and grade 3 for three patients (9%). The most common additional information from C-arm CT scans of the RIPA was the differentiation between the tumor and the systemic-to-pulmonary shunt. A systemic-to-pulmonary shunt from the RIPA was observed in 22 patients (69%), and the most common feeder of a systemic-to-pulmonary shunt was the azygoesophageal branch.
Conclusions
C-arm CT of the RIPA provides additional imaging information for the differentiation of a tumor from a nontumorous condition during chemoembolization for HCC with a suspected blood supply from an RIPA.
Abbreviations: Az, area under the receiver operating characteristic curve, DSA, digital subtraction angiography, HCC, hepatocellular carcinoma, RIPA, right inferior phrenic artery
HEPATOCELLULAR carcinoma (HCC) is a leading cause of morbidity and mortality worldwide. The incidence of HCC is on the increase due to an increasing incidence of viral hepatitis (1). Many patients have large or multiple tumors that are not amenable to surgical resection at the initial presentation. Transcatheter arterial chemoembolization is the most widely used primary treatment for unresectable HCCs (2, 3), and new intraarterial therapy using drug-eluting beads or radioactive beads has emerged with promising initial results (4, 5, 6, 7).
Three-dimensional rotational digital subtraction angiography (DSA) has been predominantly used in neuroangiographic applications to delineate the vascular anatomy (8, 9, 10). Recent technical innovations, however, have permitted three-dimensional rotational C-arm computed tomographic (CT) scans to be reconstructed by using soft tissue windows, providing CT-like images with a flat-panel DSA unit. Several studies have shown the usefulness of C-arm CT during chemoembolization by providing additional information about the vascular anatomy and tumor detection and by increasing operator confidence of the catheter position (11, 12, 13, 14).
In practice, we frequently encounter HCCs supplied by extrahepatic collateral arteries, even when the hepatic artery is patent. The right inferior phrenic artery (RIPA) is the most common extrahepatic collateral vessel that supplies HCCs (15, 16, 17). We performed this study to determine whether C-arm CT of the RIPA offers additional information during chemoembolization for HCCs with a suspected blood supply from the RIPA.
Materials and Methods
Patients
Our institutional review board approved this prospective study, and informed consent was obtained from all patients. From December 2007 to April 2008, C-arm CT of the RIPA was prospectively performed in 32 patients with HCCs that were suspected of having a blood supply from the RIPA. The patient population consisted of 27 men and five women (age range, 48–80 years; mean age, 64 years). A diagnosis of HCC was determined based on results of percutaneous needle biopsy (n = 4), surgical resection (n = 3), or laboratory testing (eg, the determination of an elevated serum α-fetoprotein level) in combination with typical CT and angiographic appearances and disease progression on follow-up images (n = 25). All 32 patients underwent contrast medium–enhanced multiphasic CT 1–3 weeks before chemoembolization.
All patients were suspected of having a blood supply from the RIPA for the following reasons: An HCC was located in the dorsal hepatic area (segment VII and VIII), as depicted on a CT scan; iodized oil infused at a previous chemoembolization session had not accumulated in the dorsal portion of the tumor as seen on CT images; even though a viable tumor abutting the diaphragm was observed in the ventral hepatic portion on CT images, correspondent tumor staining was not found at hepatic, internal mammary, and intercostal angiography; and a large RIPA was noted on a CT scan.
Chemoembolization and Imaging System
The study was performed in an interventional procedure room equipped with a commercially available DSA unit (AXIOM Artis dTA/VB30; Siemens, Erlangen, Germany). Two interventional radiologists (H.C.K., with 3 years of clinical practice, and J.W.C, with 16 years of clinical practice) performed all angiographic examinations. When selective catheterization had been achieved by placing a microcatheter with a 2.4-F tip (Microferret; Cook, Bloomington, Indiana) or 2.0-F tip (Progreat; Terumo, Tokyo, Japan) as close as possible to a specific branch or branches supplying a tumor, iodized oil (Lipiodol; Andre Gurbet, Aulnay-sous-Bois, France) and doxorubicin hydrochloride (Adriamycin RDF; Ildong Pharmaceutical, Seoul, Korea) emulsion were infused until stasis was achieved. If initial blockade of the feeding artery was insufficient due to a large mass size or arterioportal shunting, embolization was performed by using 1-mm-diameter absorbable gelatin sponge particles (Gelfoam; Upjohn, Kalamazoo, Michigan) soaked in a mixture of 2 mg of crystalline mitomycin (Mitomycin-10; Kyowa Hakko Kogyo, Tokyo, Japan) 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.
A single series of three-dimensional rotational C-arm angiographic images of the RIPA was obtained during a breath-hold, with 211° of circular trajectory for 8 seconds. With use of a power injector, contrast medium (Pamiray 300; Dongkook Pharmaceutical, Seoul, Korea) was injected at a flow rate of 1–2 mL/sec for 12 seconds, with x-ray started 4 seconds after injection. The parameters of C-arm CT were as follows: 0.5° increment, 512 × 512 matrix in projections, 211° total angle and approximately 26° per second, a system dose of approximately 0.36 μGy per frame, and a total of 419 projections. Acquired images were transferred to a commercially available dedicated workstation (Leonardo with DynaCT; Siemens), where three-dimensional CT-like images were reconstructed within 1 minute.
Data Analysis
Tumor size was defined as the largest tumor diameter determined on transverse CT scans. Tumors were assigned to liver segments in accordance with the Couinaud classification (18). If a tumor occupied two or more segments, its location was assigned to the dominant segment. In terms of multiplicity, tumors were classified as single nodular, multinodular, or infiltrative type.
Two interventional radiologists (H.C.K., J.W.C) were questioned as to whether the additional information provided with C-arm CT was useful for therapeutic decision-making or operator confidence immediately after each procedure. The judgments were obtained by consensus. The answers of these radiologists for each patient were scored as follows: grade 1 = C-arm CT provided no additional information; grade 2 = C-arm CT provided more information without an effect on the treatment plan; and grade 3 = C-arm CT provided useful information and the treatment plan was changed. The radiologists also recorded the presence or absence of tumors and the presence or absence of a systemic-to-pulmonary shunt from the RIPA by consensus. Tumor feeders and feeders of a systemic-to-pulmonary shunt were recorded (Fig 1). Complications such as shoulder pain and pulmonary oil embolization were recorded.
Figure 1.
Images in a 48-year-old man with HCC invading the inferior vena cava. (a) Right inferior phrenic arteriogram obtained at the first session of chemoembolization shows hypervascular tumor staining in the liver dome (solid white arrow) and tumor staining in the inferior vena cava (+) supplied by the RIPA. Note the anterior branch (open white arrow), posterior branch (open black arrow), azygoesophageal branch (open arrowheads), pericardiophrenic branch (solid black arrow), and superior adrenal artery (solid arrowhead). Systemic-to-pulmonary shunts (star) along the lung base supplied by the azygoesophageal branch are noted. (b,c) Contrast-enhanced C-arm CT scans show the enhancing pulmonary arteries and lung parenchyma (solid arrows). Note the anterior branch (open arrows), azygoesophageal branch (solid arrowheads) toward the medial azygoesophageal recess below the diaphragm, and azygoesophageal branch (open arrowheads) toward the lateral costophrenic angle above the diaphragm.
We also assessed the individual performance of radiologists who did not take part in the C-arm CT procedures with regard to the presence or absence of tumors and systemic-to-pulmonary shunts from the RIPA. Two radiologists (J.H.P., with 27 years of clinical experience in an academic practice, S.A., a senior resident with a clinical experience of performing approximately 300 chemoembolization procedures), independently reviewed the conventional DSA and C-arm CT images. These clinicians assigned one of five confidence level ratings for the presence or absence of tumors and a systemic-to-pulmonary shunt from the RIPA, as follows: 1 = definitely absent, 2 = probably absent, 3 = indeterminate, 4 = probably present, 5 = definitely present.
The individual performances of the radiologists with respect to the presence or absence of tumors and the presence or absence of systemic-to-pulmonary shunts from the RIPA were evaluated and compared by using the area under the receiver operating characteristic curve (Az). P values less than .05 were regarded as statistically significant. Statistical analysis was performed by using commercially available software (MedCalc, version 7.4.4.1; MedCalc Software, Mariakerke, Belgium).
Results
Tumor sizes ranged from 1.1 to 14 cm (mean size, 3.8 cm). Tumors were located in segment VII (n = 16), segment VIII (n = 12), segment IV (n = 3), and segment II (n = 1). Nine tumors were classified as single nodular, 20 as multinodular, and three as infiltrative. Tumor thrombi within the inferior vena cava were noted in four patients. All hepatic tumors abutted the liver surface or the diaphragm. Right inferior phrenic angiography was performed during the first to the 19th (mean, 6.1 sessions; median, 5 sessions) chemoembolization session; it was performed during the first session in seven patients (22%) and during a repeated session in 25 (78%).
Thirty-one patients showed tumor staining at hepatic angiography, and 22 patients had tumors fed by the RIPA. One patient had tumors exclusively supplied by the RIPA. Twenty-one patients had tumors supplied by both the hepatic artery and the RIPA. Angiography of the RIPA showed tumor staining (n = 7), a systemic-to-pulmonary shunt (n = 7), both tumor staining and a systemic-to-pulmonary shunt (n = 15), and neither tumor staining nor a systemic-to-pulmonary shunt (n = 3). Chemoembolization via the hepatic artery was performed in 31 patients, and chemoembolization via the RIPA was undertaken in 21 patients. Chemoembolization via the RIPA was not performed in one patient because a severe systemic-to-pulmonary shunt from the RIPA was present despite the presence of tumor staining fed by the RIPA.
Tumor feeders from the RIPA in 22 patients included the anterior branch (n = 10), posterior branch (n = 5), anterior and posterior branch (n = 4), posterior and superior adrenal branch (n = 1), superior adrenal branch (n = 1), and azygoesophageal branch (n = 1). Forty-two feeders of systemic-to-pulmonary shunts were noted in 22 patients, including the azygoesophageal branch (n = 18), anterior branch (n = 13), posterior branch (n = 9), and pericardiophrenic branch (n = 2).
During the procedures, all patients who received chemoembolization via the RIPA complained of a variable degree of right shoulder pain. Pulmonary oil embolization was noted in five patients, and two of the patients complained of transient chest tightness. Pleural effusion was noted in two patients on a follow-up CT scan, but no specific treatment was needed.
The information provided with C-arm CT was classified as grade 1 for nine of the 32 patients (28%), grade 2 for 20 (63%), and grade 3 for three (9%). The grade 3 information was as follows: (a) C-arm CT enabled the confirmation of tumor staining that was ambiguous at conventional DSA (n = 2) (Fig 2) and (b) C-arm CT demonstrated no tumor staining fed by the RIPA (n = 1). The grade 2 information was as follows: C-arm CT provided increased operator confidence of tumor staining (n = 8) or demonstrated the presence of a systemic-to-pulmonary shunt (n = 6), increased operator confidence in determining the absence of tumor staining fed by the RIPA (n = 5) (Fig 3), and provided visualization of an arterioportal shunt (n = 3) or a phrenic artery-to-hepatic vein shunt (n = 1). C-arm CT also provided demonstration of partial tumor staining fed by the RIPA with a severe systemic-to-pulmonary shunt (n = 1), visualization of a small feeding vessel to the tumor (n = 1), or identification of an accessory renal polar artery with renal parenchymal staining (n = 1).
Figure 2.
Images in an 80-year-old man with HCC supplied by the RIPA. (a) Transverse CT scan obtained during the hepatic arterial phase shows a small hypervascular tumor (arrowheads) in segment VII. Note the previously infused iodized oil (arrows). (b) Transverse CT scan obtained during the hepatic arterial phase shows a hypervascular retroperitoneal lymph node (arrowhead) suggestive of nodal metastasis. Note the previously infused iodized oil (arrow). (c) Transverse CT scan obtained during the hepatic arterial phase shows a small hypervascular tumor (arrowheads) in segment VI. Note the previously infused iodized oil (arrow). (d) Right inferior phrenic arteriogram obtained at the 8th session of chemoembolization shows hypervascular tumor staining in segment VII (solid black arrow), hypervascular tumor staining beside the inferior vena cava (open white arrow), and retroperitoneal nodal metastasis (arrowhead). Note ill-defined ambiguous staining (open black arrow). Celiac angiography revealed no tumor staining supplied by the hepatic artery (not shown). (e) Contrast-enhanced C-arm CT scan shows enhancement of the tumor in segment VII (arrowhead) and the tumor beside the inferior vena cava (arrow). (f) Contrast-enhanced C-arm CT scan shows enhancement of the retroperitoneal lymph node (arrowhead). Note the previously infused iodized oil (arrow). (g) Contrast-enhanced C-arm CT scan shows enhancement of the tumor in segment VI (arrowhead), which was ambiguous at DSA. Note the previously infused iodized oil (arrow).
Figure 3.
Images in a 50-year-old man with HCC supplied by the right hepatic artery. (a) Transverse CT scan obtained during the hepatic arterial phase shows a small exophytic hypervascular tumor (arrowhead) in segment VIII. (b) Right inferior phrenic arteriogram obtained at the first session of chemoembolization shows no hypervascular tumor staining. Note the pulmonary arteries (arrows) within systemic-to-pulmonary shunt staining and the azygoesophageal branch (arrowheads). (c) Contrast-enhanced C-arm CT scan shows no enhancement of tumor in segment VIII. The RIPA (arrowheads) is noted. (d) Contrast-enhanced C-arm CT scan shows enhancement of the pulmonary arteries (arrowheads).
The individual performance of radiologists who did not take part in C-arm CT procedures with regard to the presence or absence of tumors and systemic-to-pulmonary shunts from the RIPA are summarized in Table. Whereas the performance of the experienced radiologist for detecting a tumor and systemic-to-pulmonary shunt from the RIPA did not improve with the use of C-arm CT, the performance of the inexperienced radiologist improved; the finding was not of statistical significance.
Radiologist Performance for the Presence or Absence of Tumor and Systemic-to-Pulmonary Shunt from a RIPA
| Radiologist⁎ | Tumor | Systemic-to-Pulmonary Shunt | ||||
|---|---|---|---|---|---|---|
| DSA† | C-arm CT† | P Value‡ | DSA† | C-arm CT† | P Value‡ | |
| Radiologist 1 | 0.925 (0.774,0.987) | 0.932(0.784,0.989) | .898 | 0.914(0.759,0.982) | 0.914(0.759,0.982) | .999 |
| Radiologist 2 | 0.745(0.561,0.862) | 0.823(0.647,0.934) | .430 | 0.773(0.591,0.901) | 0.868(0.701,0.960) | .197 |
⁎Radiologist 1 was an attending staff with 27 years of clinical experience, and radiologist 2 was a senior resident with clinical experience of about 300 chemoembolization procedures. |
†Data are given as Az values. Numbers in parentheses are 95% confidence interval. |
‡Two-tailed P values between the Az values of both radiologists for DSA and C-arm CT were calculated with a univariate z score test. |
The radiation dose of a single series of three-dimensional rotational C-arm CT scans ranged from 79.9 mGy to 219.0 mGy (mean, 151.4 mGy), and the total radiation dose of the chemoembolization procedure ranged from 206.1 mGy to 647.2 mGy (mean, 383.7 mGy).
Discussion
The combination of vascular and soft tissue depiction of C-arm CT has potential benefits in the performance of chemoembolization, as the relationship of the targeted tumor with its arterial supply can be clearly identified (11, 12, 13, 14). Our results showed that C-arm CT of the RIPA provided additional information for 23 of 32 patients (72%) and resulted in a change in the procedure for three (9%). In this series, interestingly, a systemic-to-pulmonary shunt from the RIPA was observed in 22 of the 32 patients (69%). C-arm CT of the RIPA was helpful for the inexperienced radiologist in the detection of tumor staining and a systemic-to-pulmonary shunt from the RIPA.
The most common additional information obtained from C-arm CT scans of the RIPA was the differentiation between the tumor and a systemic-to-pulmonary shunt. Webb and Jacobs (19) described a vascular blush caused by transpleural systemic-pulmonary arterial anastomosis, and a systemic-to-pulmonary shunt can be confused as tumor staining (20). If the shunt is massive, it is relatively simple to differentiate pulmonary staining from tumor staining with visualization of the lower lung margin and draining of the pulmonary veins at DSA (20). However, the small systemic-to-pulmonary shunt can sometimes be shown as just small ill-defined staining at DSA and be mistaken as tumor. Whereas tumors fed by the RIPA were seen as enhancing lesions in the liver on the C-arm CT images, systemic-to-pulmonary shunts from the RIPA were observed as enhancing pulmonary vessels on the C-arm CT images. In our study, 15 patients showed both tumor staining and a systemic-to-pulmonary shunt from the RIPA. In these cases, we believe that the use of C-arm CT is more helpful for differentiating exactly between the extent of tumor staining and pulmonary staining.
In our study, a systemic-to-pulmonary shunt from the RIPA was noted in 22 patients (69%). Tajima et al (21) reported that three of 44 patients (7%) had a systemic-to-pulmonary shunt from the RIPA. The prevalence of a systemic-to-pulmonary shunt from the RIPA is unknown and may be overestimated in our study because many patients with a large RIPA depicted at CT may be included in our study. We think that the quality of the angiographic images of the newer angiographic unit employed in our study is very high so that a small systemic-to-pulmonary shunt, which could not be observed on older angiographic units, can be visualized on DSA and C-arm CT images.
Although the most common tumor feeder was the anterior branch, the most common feeder of a systemic-to-pulmonary shunt was the azygoesophageal branch. Although the azygoesophageal branch is not frequently described in anatomy textbooks or reports, we have frequently observed the typical course of the azygoesophageal branch supplying a systemic-to-pulmonary shunt. It usually arises from the RIPA at the proximal portion of the anterior branch and courses medially, undergoes a U-turn at the medial end of azygoesophageal recess, and then courses laterally along the costophrenic angle of the lung base. On C-arm CT images, the azygoesophageal branch penetrates the diaphragm at the U-turn point, and an enhancing pulmonary artery is noted in the azygoesophageal recess and posteromedial lung base.
Chemoembolization through the RIPA frequently results in pulmonary complications, including iodized oil accumulation in the lung field, consolidation, pleural effusion, and atelectasis (21, 22, 23). Most patients with pulmonary complications are asymptomatic, but symptomatic pulmonary embolism and pulmonary infarction occur in some cases (21, 24). Chemoembolization of the RIPA causes right shoulder pain in most cases. To reduce shoulder pain, it is recommended that a small amount of 1% lidocaine be injected intraarterially during embolization of the RIPA. In patients who have both tumors and systemic-to-pulmonary shunts from the RIPA, selective catheterization via the tumor feeder is necessary to avoid pulmonary oil embolization. If selective catheterization fails and the systemic-to-pulmonary shunt is massive, we first infuse Gelfoam particles to reduce the size of the systemic-to-pulmonary shunt and then infuse iodized oil. If selective catheterization is not possible and the systemic-to-pulmonary shunt is not massive, we first infuse iodized oil and then infuse Gelfoam particles, as the small amount of pulmonary oil embolization usually does not cause pulmonary symptoms. In our study, 15 patients had both tumor staining and a systemic-to-pulmonary shunt from the RIPA; pulmonary oil embolization was observed in five patients. Although two of the patients complained of transient chest tightness, it did not cause any clinical problem. Because even a small systemic-to-pulmonary shunt can be visualized on C-arm CT images, possible pulmonary complications can be reduced with a careful search for a systemic-to-pulmonary shunt.
The performance of the experienced radiologist in the detection of a tumor and systemic-to-pulmonary shunt from the RIPA did not improve with the use of C-arm CT, as the experienced radiologist was able to detect tumors and a systemic-to-pulmonary shunt with DSA only in most cases and the experienced radiologist was not familiar with the C-arm CT images. C-arm CT was helpful for inexperienced radiologist in the detection of tumors and shunts, despite the lack of statistical significance. We think that the diagnostic performance was not statistically significant due to the small number of patients in this study.
Tumor thrombi in the inferior vena cava can be frequently supplied by the RIPA. According to a recent report (25), 54 (66%) of the 82 patients who had tumor thrombi in the inferior vena cava had extrahepatic collateral arterial supply, 47 of which were from the RIPA. In our study, four patients had tumor thrombi within the inferior vena cava.
There are some limitations of the present study. First, the study population was small, so the performance of C-arm CT was not statistically significant. Second, we did not determine the effect of C-arm CT on radiation exposure, procedural time, and increased contrast medium load to the patient. This determination would require a control arm of patients treated without C-arm CT. Third, there was a selection bias. We performed selective angiography of the RIPA with suspicion of blood supply. Patients with a large RIPA depicted on a CT scan could easily be included in our study so that the prevalence of a systemic-to-pulmonary shunt might be overestimated because the RIPA can often be dilated due to the presence of a systemic-to-pulmonary shunt.
In conclusion, our results indicate that the use of C-arm CT of the RIPA can improve the detection of tumor staining and a systemic-to-pulmonary shunt. A systemic-to-pulmonary shunt from the RIPA can be frequently observed at C-arm CT, and the most common feeder of a systemic-to-pulmonary shunt was the azygoesophageal branch. C-arm CT of the RIPA was more helpful for the inexperienced radiologist with regard to the detection of tumor staining and a systemic-to-pulmonary shunt from the RIPA.
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None of the authors have identified a conflict of interest.
PII: S1051-0443(09)00336-4
doi:10.1016/j.jvir.2009.03.036
© 2009 SIR. Published by Elsevier Inc. All rights reserved.
Volume 20, Issue 7 , Pages 888-895, July 2009
