|Year : 2017 | Volume
| Issue : 1 | Page : 38-43
Dual phase cone-beam computed tomography in detecting <3 cm hepatocellular carcinomas during transarterial chemoembolization
Xiaodong Wang1, Hooman Yarmohammadi2, Guang Cao1, Xinqiang Ji3, Jungang Hu1, Hirad Yarmohammadi4, Hui Chen1, Xu Zhu1, Renjie Yang1, Stephen B Solomon2
1 Department of Interventional Radiology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China
2 Department of Radiology, Interventional Radiology Service, Memorial Sloan-Kettering Cancer Center, New York, USA
3 Department of Medical Statistics, Peking University Cancer Hospital and Institute, Beijing, China
4 Department of Medicine, University of Minnesota, Minneapolis, Minnesota, USA
|Date of Web Publication||16-May-2017|
Department of Radiology, Division of Interventional Radiology, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York 10065
Source of Support: None, Conflict of Interest: None
Objective: The objective of this study was to evaluate the sensitivity of dual phase cone-beam computed tomography (CBCT) in detecting small (<3 cm in diameter) hepatocellular carcinoma (HCC) tumors during transarterial chemoembolization (TACE).
Materials and Methods: Twenty-two consecutive patients with unresectable small HCCs in whom TACE was performed were retrospectively evaluated. Contrast CT or contrast magnetic resonance imaging (MRI) was performed in all patients within 1 month prior to the procedure. Dual phase CBCT was performed prior to TACE and lipiodol-CBCT was performed after treatment. The sensitivity of dual phase CBCT in detecting small HCCs was compared to hepatic angiography, contrast enhanced CT and MRI.
Results: Seventy HCC tumors with sizes of <3 cm were detected in 22 patients. Dual phase CBCT depicted 67 small tumors either on arterial or venous phase and was significantly more sensitive compared to hepatic angiography, contrast CT, or MRI (95.7%, 65.7%, and 71.4%, respectively; P < 0.001).
Conclusions: Dual phase CBCT is significantly more sensitive than hepatic angiography, contrast enhanced CT, and MRI in detecting smaller than 3 cm HCC tumors and can be a helpful modality in making accurate planning for treatment of HCC.
Keywords: Cone-beam computed tomography, digital subtraction angiography, hepatic arteriography, hepatocellular carcinoma, transarterial chemoembolization
|How to cite this article:|
Wang X, Yarmohammadi H, Cao G, Ji X, Hu J, Yarmohammadi H, Chen H, Zhu X, Yang R, Solomon SB. Dual phase cone-beam computed tomography in detecting <3 cm hepatocellular carcinomas during transarterial chemoembolization. J Can Res Ther 2017;13:38-43
|How to cite this URL:|
Wang X, Yarmohammadi H, Cao G, Ji X, Hu J, Yarmohammadi H, Chen H, Zhu X, Yang R, Solomon SB. Dual phase cone-beam computed tomography in detecting <3 cm hepatocellular carcinomas during transarterial chemoembolization. J Can Res Ther [serial online] 2017 [cited 2022 Jun 29];13:38-43. Available from: https://www.cancerjournal.net/text.asp?2017/13/1/38/206242
| > Introduction|| |
Hepatocellular carcinoma (HCC) is the 6th most common cancer and the 3rd leading cause of cancer-related death worldwide. Transarterial therapy has been proved to be an effective local tumor therapy in patients with unresectable disease.
One of the most common reasons for early recurrence after treatment is the inability to identify all lesions including the small or occult tumors prior to treatment. Therefore, detection of all tumor nodules, including the smaller HCCs (<3 cm), is essential in achieving best treatment results. Unfortunately, angiography frequently cannot detect small HCC lesions. In addition, conventional tri- or bi-phasic contrast enhanced computed tomography (CT) and magnetic resonance imaging (MRI) are less sensitive in detecting small lesions.
The high spatial resolution of C-arm cone-beam CT (CBCT) using a flat-panel and three-dimensional (3D) angiography has been increasingly used in the past several years to delineate occult liver tumors and to identify intrahepatic or extrahepatic arterial supply to a tumor with a performance comparable to CT angiography.,,, However, due to varied parameters of contrast injection including injection volume, injection concentration (diluted vs. full strength), injection rate (cc/s), scan timing delay of the arterial phase, and venous phase acquirement the performance of the so-called dual phase CBCT varies significantly.
The objective of this study was to compare the sensitivity of dual phase CBCT, using optimized parameters, in detecting small HCC tumors (<30 mm) with hepatic arterial digital subtraction angiogram and contrast enhanced tri-phase CT or MRI.
| > Materials and Methods|| |
A waiver of authorization was obtained from the Institutional Review Board for this retrospective study. Between September 2011 and July 2012, 22 consecutive patients with unresectable HCC that were treated with transarterial chemoembolization (TACE) and met the inclusion criteria were enrolled. The inclusion criteria were (1) patients who sequentially underwent nonselective hepatic arteriography, dual phase CBCT, lipiodol-TACE, and lipiodol-CBCT; (2) patients with at least one tumor <30 mm; and (3) patients without diffuse liver tumor. All patients had a contrast enhanced CT or MRI within 1 month prior to TACE procedure. Patients with hepatic arterial variations with at least two separate hepatic arteries arising from the abdominal aorta and those with a history of hepatic resection were excluded from the study.
Nonselective hepatic arterial digital subtraction angiogram was performed in the anteroposterior projection on injection of the common or proper hepatic artery with iodinated contrast (Xeneti × 350, Aulnay-Sous-Bois, France) 4–5 ml/s for 4–5 s. A 40 cm flat panel angiography system (Innova 4100, GE Healthcare, Waukesha, WI, USA) was used.
Dual-phase cone-beam computed tomography technique
After the two-dimensional (2D) DSA study, a 3D CBCT was performed with injection of the common or proper hepatic artery. A total of 27–36 ml of Xeneti × 350 was injected at a rate of 3–4 ml/s for 9 s, with a delay time of 4.5 s and 55 s for arterial phase and venous phase acquisition, respectively. One hundred and fifty projection images were obtained during a 5 s acquisition with 180° rotation (40°/s) around the region of interest for arterial phase CBCT scan. Two hundred and ninety-three projection images were obtained during a 10 s acquisition with 180° rotation (20°/s) for the venous phase scan. CBCT cross-sectional images with matrix size of 512 × 512 × 512 were reconstructed from the projections. Afterward, 1.8 mm thick CBCT axial images were obtained.
TACE was performed using the previously described technique., After the TACE procedure, a CBCT scan was acquired with 180° rotation, 20°/s for 10s. CBCT cross-sectional images with matrix size of 512 × 512 × 512 were reconstructed from the projections.
Two radiologists, blinded to the study, retrospectively evaluated all the CT or MRI, DSA, dual phase CBCT, and lipiodol-CBCT images. The imaging criteria for the diagnosis of HCC on contrast enhanced CT and MRI was contrast enhancement on arterial phase and washout on venous phase. The diagnosis of HCC on arterial phase and venous phase CBCT was tumor staining and washout with or without coronal enhancement, respectively.
Sensitivity of dual phase CBCT, hepatic angiography, and contrast enhanced CT or MRI for the detection of HCC lesions was calculated as the consensus of positive tumor nodules detected on arterial phase, venous phase, and dual phase CBCT, hepatic angiography, contrast-enhanced CT or MRI divided by the actual number of HCC nodules detected on the gold standard imaging.
Statistical analysis was performed using SPSS (version SPSS 17.0, Polar Engineering and Consulting, Chicago, IL, USA). A Chi-squared test was used to compare the detection rate of dual phase CBCT, hepatic angiography, contrast enhanced CT or MRI. P< 0.05 was considered as statistically significant.
| > Results|| |
Twenty-two patients with mean age of 60.9 ± 10.96 years (range: 46–82 years; 21 male and 1 female) were evaluated. Patient demographics and tumor characteristics are listed in [Table 1]. Seventy small hepatic carcinoma tumors with a mean size of 12.2 ± 7.5 mm (range: 3.6–30 mm) were detected. Thirty-five tumors were detected on contrast enhanced CT, 15 on contrast enhanced MRI, 44 on angiography and/or CBCT + corona enhancement on CBCT and 61 tumors on angiography and/or CBCT + dense accumulation of lipiodol after chemoembolization.
|Table 1: Baseline characteristics of patients with hepatocellular carcinoma and characteristics of all small tumors|
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Dual phase CBCT depicted 95.7% of small tumors (67 of 70 tumors) either on arterial or venous phase. The sensitivity of arterial phase CBCT was much higher than that of venous phase (92.9% vs. 68.9%; P< 0.001). Of the 70 small tumors, 19 were detected only on arterial phase CBCT, rather than on venous phase. Only two were detected just on venous phase rather than on arterial phase. For smaller nodules which were <10 mm, the sensitivity of arterial phase CBCT was significantly higher than the venous phase (94.3% vs. 42.9%, P< 0.001). For nodules larger than 10 mm, the sensitivity of these two phases were similar (91.4% vs. 94.3%; P = 1.0). On the venous phase, the corona enhancement was shown in 46 (68.6%) of all 67 lesions, and 46 (95.8%) of 48 venous phase visualized tumors. The mean tumor diameter with corona enhancement was 14.5 ± 7.9 mm. The minimal tumor size with corona enhancement was 4.2 mm in diameter. Six wedge shape or irregular stained areas (size = 12.8 ± 7.0 mm) that were depicted on the arterial phase CBCT were not detected on venous phase and did not show dense lipiodol accumulation on lipiodol-CBCT. These were deemed as portal venous fistula.
The sensitivity of hepatic angiography was 65.7%. DSA was less sensitive (51.4%) in detecting lesions <10 mm.
The sensitivity of preprocedure CT or MRI was 71.4%. Smaller the lesions lower the sensitivity on contrast enhanced CT or MRI [Figure 1] and [Figure 2]. In regards to the 35 < 10 mm tumors, preprocedural CT or MRI only depicted twenty (57.1%) tumors, as shown in [Table 2].
|Figure 1: A 55-year-old male patient with multifocal hepatocellular carcinoma (Child-Pugh class A). (a) Demonstrates the arterial phase contrast enhanced-magnetic resonance imaging showing two enhancing masses in liver segments 1 and 5 (white arrows). (b) Contrast enhanced magnetic resonance imaging of the same patient from segment 6 of the liver demonstrating no definite tumor in this area. (c and d) Venous phase contrast enhanced-magnetic resonance imaging at the same corresponding axial slice levels showing washout of the two tumors in segment 1 and 5 (white arrows), but no definite finding in segment 6. (e and f) Arterial phase cone-beam computed tomography of the dual phase cone-beam computed tomography performed prior to transarterial chemoembolization at the same axial levels that demonstrate the two hypervascular tumors in segment 1 and 5 (white arrows) corresponding to the contrast enhanced-magnetic resonance imaging findings. In addition, a 5.6 mm enhancing tumor is detected in segment 6 (white arrow) not previously identified in the contrast enhanced-magnetic resonance. (g and h) Venous phase dual-phase cone-beam computed tomography images demonstrating the internal washout of the three tumors with peripheral corona enhancement including the small lesion in segment 6 (white arrow). (i and j) Lipiodol-cone-beam computed tomography immediately after transarterial chemoembolization demonstrating the high intense tumors (white arrows)|
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|Figure 2: Images of a 51-year-old male with diffuse hepatocellular carcinoma in the right lobe (Child-Pugh class A). (a and b) Arterial and venous phase contrast enhanced-magnetic resonance imaging demonstrating no visible lesion in the left lobe. (c) Hepatic artery angiography demonstrates no lesions in the left lobe. (d) Arterial phase cone-beam computed tomography prior to transarterial chemoembolization at the same axial levels of contrast enhanced-magnetic resonance imaging identifying one enhancing tumor (white arrow) in segment 2, and another enhancing lesion (black arrow) in segment 1. (e) Venous phase cone-beam computed tomography demonstrating the internal washout (white arrow) with peripheral corona enhancement for the lesion in segment 2, and isodensity (black arrow) for the lesion in segment 1|
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|Table 2: Sensitivity of contrast enhance computed tomography and magnetic resonance imaging, hepatic artery digital subtraction angiogram, and dual phase cone-beam computed tomography for small hepatocellular carcinoma tumors and comparison between the three groups|
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Dual phase CBCT was able to significantly detect higher numbers of tumor compared to CT or MRI (P < 0.001) [Figure 1] and [Figure 2]. In addition, it was more sensitive than 2D hepatic angiography (P < 0.001) [Table 2]. When the tumors were subdivided into two groups of smaller than 1 cm and larger than 2 cm, this difference was only significant for lesions <1 cm (P = 0.002, and P = 0.001, respectively).
Dual phase CBCT was able to change the intra-procedure decision and treatment strategy in 38.6% (27) of the lesions: Initial lobar TACE was changed to segmental treatment in nine (12.9%) of the lesions and initial plan of segmental TACE was changed to super-selective (via selective feeding artery) treatment in 18 (25.7%) of the lesion. One lesion (1.4%) was not detected during TACE and was only detected during the retrospective analysis. Dual phase CBCT had not influenced on the treatment plan of the remaining 42 (60%) lesions.
| > Discussion|| |
The above study demonstrates that CBCT and 3D vessel imaging using flat-panel detector provides additional critical information for patients undergoing TACE.,,, This is similar to previous studies by Miyayama et al. in which C-arm CBCT using a flat-panel and 3D angiography were used to delineate occult liver tumors with a performance comparable to conventional CT angiography.,
Compared to single-phase CBCT, dual phase CBCT, including a hepatic arterial phase and an arterioportal phase CBCT provides more dynamic information in regards to tumor detection and assistance with accurate diagnosis of HCC. However, dual phase CBCT requires two separate image acquisitions in the hepatic artery or the superior mesenteric artery., Dual phase CBCT also could provide superior liver tumor conspicuity and recent studies have reported greater sensitivity of tumor detection compared to single phase hepatic artery CBCT.,,, In the present study, the sensitivity of dual phase CBCT in detecting small HCC tumors (<30 mm) was 95.7%, which was significantly higher than that of contrast enhanced CT or MRI. Similarly, Loffroy et al. reported a 93.9% detection rate of 82 MRI confirmed HCC tumors on dual phase CBCT. In that study, combined dual-phase acquisition improved detectability of HCC lesions compared with the single-phase studies and had the ability to detect almost all HCC tumors. The higher sensitivity of dual phase CBCT in detecting tumors was translated into change of the intra-procedure decision and treatment strategy in 38.6% (27) of the lesions which is a very important observation.
One of the advantages of the current study is the explicitly defined acquisition technique and the timing that was meticulously executed. Loffroy et al. injected contrast in the early arterial phase and later arterial phase and therefore, the dual phase CBCT was not divided into an arterial and venous phase. This may result in less tumor staining in the early arterial phase. In the present study, tumor stain on the arterial phase CBCT was pronounced and the venous phase was used to show the washout with or without corona enhancement providing additional confirmation.
Review of the literature demonstrates a variety of performances reported on dual-phase CBCT with no universal or standard contrast injection, scan time, or acquirement parameter.,, The parameter of contrast injection used in the current study was 27–36 ml of undiluted contrast at a rate of 3–4 ml/s for 9 s and 4.5 s delay for the arterial phase CBCT acquisition and 55 s delay for venous phase acquisition. These parameters were set for better visualization of both tumor-feeding vessels and tumor stain on the arterial phase. The 55 s delay set for venous phase acquisition was to achieve better visualization of the contrast washout of the tumor on the venous phase. The rotation speed of 40°/s was deemed sufficient to depict the vessels and tumor stain on arterial phase and 20°/s was applied to show superior soft tissue resolution when the contrast was almost completely washed out from the field of view on the venous phase. In the present study, the sensitivity of arterial phase CBCT was 92.9% which was higher than similar recent studies and is most likely related to the timing of contrast injection. Another important finding of the present study is that the venous phase CBCT showed contrast washout and corona enhancement much better than tumor stain emphasizing the importance of contrast injection. In the Loffroy et al. study, the venous phase (equivalent to a late arterial phase) demonstrated a higher sensitivity of detecting tumor stain (86.6%).
Corona enhancement is one of the characteristic findings of hypervascular HCC on late-phase CT during hepatic arteriography and single-level dynamic CT angiography.,, Histological studies have showed that corona enhancement of HCC tumor represented drainage from the tumor sinusoids to the surrounding liver sinusoids. When there was a thick corona enhancement, it represented the tumor blood drainage into surrounding liver parenchyma through the preserved portal veins within the capsule. On single-level dynamic CT angiography, corona enhancement around the HCC lesion appears between 22 and 40 s after contrast injection. In the current study, the corona enhancement was shown in 65.7% of all small lesions, and in almost all visualized tumors on venous phase (95.8%). The mean tumor diameter with corona enhancement was 14.5 ± 7.9 mm and minimal tumor size with corona enhancement was 4.2 mm. Although the corona enhancement was rarely seen in very small lesions with <10 mm diameter, it definitely helped to distinguish between HCC and other hypervascular lesions, such as arterioportal shunts or dysplastic nodules., The very low visualization of corona enhancement in very small lesions (<10 mm) is possibly due to the tumor growth pattern or relatively low-density resolution of CBCT. Miyayama et al. reported that 88.7% of hypervascular HCC lesions were depicted with corona enhancement on the second phase of the dual phase CBCT. This is higher than what was detected in the present study (65.7%). This may be due to the fact that Miyayama et al. evaluated larger tumors (<5 cm, mean 2.4 ± 1.7 cm) compared to the present study (<3 cm, mean 12.2 ± 7.7 mm).
The contrast enhanced CT or MRI is the most widely accepted imaging modality for diagnosing HCC. It is easily applied and is a noninvasive method. However, these modalities may underestimate small HCC nodules. Previous studies have reported that CT angiography with or without arterial phase CT, dual phase CBCT with or without arterial phase CBCT or a late phase dual phase CBCT, lipiodol CT, and lipiodol-CBCT are all superior to conventional contrast enhanced CT and MRI, specifically for occult HCC lesions.,, Multidetector hepatic arteriography CT has higher sensitivity in revealing small and multifocal HCCs when compared to contrast enhanced CT and MRI. Hepatic arteriography CT frequently resulted in altering the treatment plans involving selective administration of chemoembolic material. However, hepatic arteriography CT can be cumbersome since the hybrid angiogram-CT systems are not available everywhere, and it is troublesome to move patients from interventional suite to CT suite.
There are some limitations in this study. First, pre-TACE procedure imaging was based on contrast enhanced CT or MRI and not on a single imaging modality. Second, some contrast enhanced CT and MRIs were not performed in our center, and therefore the imaging protocols and resolutions varied. Third, there were no histological confirmations for almost all tumors. The fourth limitation of the study was a bias in patient recruitment; patients with hepatic variation were excluded from the study protocol. Finally, some CBCT images with somewhat respiratory motion artifacts may have influenced the results, which is also a limitation of CBCT compared with MDCT.
| > Conclusions|| |
Dual phase CBCT with single contrast injection is more sensitive in detecting HCC tumors of <30 mm in diameters compared to contrast enhanced CT or MRI and hepatic angiography resulting in change of intra-procedure treatment planning in approximately 40% of lesions. The sensitivity is more pronounced in tumors <10 mm. In addition, the sensitivity of arterial phase CBCT is higher than venous phase and corona enhancement on venous phase CBCT and is helpful in distinguishing between HCC and hypervascular arteriovenous shunts. Therefore, we conclude that dual phase CBCT is a helpful modality in making accurate planning for TACE and potentially for determining resectability of HCC tumors.
This project was supported by the Natural Science Foundation of China (81271671), Technology Foundation for Selected Overseas Chinese Scholar; Beijing High-Level Medical Personal Fund (2013-3-084).
Financial support and sponsorship
This projectE was supported by the Natural Science Foundation of China (81271671), Technology Foundation for Selected Overseas Chinese Scholar; Beijing High-Level Medical Personal Fund (2013-3-084).
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2]
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