- Email: [email protected]
Embolization for Bleeding after Hepatic Radiofrequency Ablation
CLINICAL STUDY
Embolization for Bleeding after Hepatic Radiofrequency Ablation Jong Woo Kim, MD, Ji Hoon Shin, MD, PhD, Pyo Nyun Kim, MD, PhD, Yong Moon Shin, MD, PhD, Hyung Jin Won, MD, PhD, Gi-Young Ko, MD, PhD, and Hyun-Ki Yoon, MD, PhD
ABSTRACT Purpose: To evaluate safety and clinical efficacy of embolization for management of bleeding after hepatic radiofrequency (RF) ablation. Materials and Methods: From January 2000 to December 2014, 5,196 patients with 9,743 tumors underwent 8,303 RF ablation sessions. Of these patients, 62 experienced bleeding after hepatic RF ablation; 15 patients (12 men and 3 women; mean age 62 y; range, 49–76 y) underwent embolization and composed the final study cohort. Tumors were hepatocellular carcinomas in 13 (87%) patients and metastatic adenocarcinomas from colorectal cancer in 2 (13%) patients. Mean number of tumors was 1.5 (22 nodules; range, 1–3). Tumor locations were segment I (n ¼ 1), segment II (n ¼ 2), segment III (n ¼ 1), segment IV (n ¼ 1), segment V (n ¼ 3), segment VI (n ¼ 5), segment VII (n ¼ 1), and segment VIII (n ¼ 9). Mean tumor size was 2.3 cm (range, 0.9–5 cm). Results: Median time interval between presentation and angiography was 22 hours (mean 38.4 h; range, 3–168 h). On angiography, contrast extravasation with or without pseudoaneurysm was seen in all 15 patients; 14 patients underwent transarterial embolization, and 1 patient underwent percutaneous transhepatic portal vein embolization. Successful hemostasis was achieved in all patients. There was no rebleeding within 30 days after embolization. No embolization-related major complications were observed. Conclusions: Embolization is safe and effective for controlling bleeding related to hepatic RF ablation without the need for surgery.
ABBREVIATION INR = international normalized ratio
Radiofrequency (RF) ablation is considered a relatively safe and minimally invasive treatment for primary and secondary hepatic neoplasms. However, it has been shown to be associated with various complications.
From the Department of Radiology (J.W.K.), Gachon University Gil Medical Center, Incheon, Korea; and Department of Radiology and Research Institute of Radiology (J.W.K., J.H.S., P.N.K., Y.M.S., H.J.W., G.-Y.K., H.-K.Y.), University of Ulsan College of Medicine, Asan Medical Center, 88, Olympic-Ro 43-Gil, Songpa-Gu, Seoul 05505, Korea. Received February 16, 2016; final revision received September 28, 2016; accepted September 29, 2016. Address correspondence to J.H.S.; E-mail: [email protected] None of the authors have identified a conflict of interest. Figures E1 and E2 are available online at www.jvir.org. & SIR, 2016 J Vasc Interv Radiol 2016; XX:]]]–]]] http://dx.doi.org/10.1016/j.jvir.2016.09.031
The estimated range of mortality rates is 0.1%–0.5%, and the estimated range of major complications is 2.2%– 3.1% (1–4). In particular, among the major adverse outcomes of RF ablation, bleeding complications, such as hemobilia, hemoperitoneum, and hemothorax, can be life-threatening if diagnosis and treatment are delayed (5–8). Thus, prompt management of such bleeding complications is essential for successful treatment using RF ablation. Embolization has been shown to have advantages over surgery for the management of bleeding complications related to RF ablation (9). However, to the best of our knowledge, reports focusing on embolization for active bleeding after hepatic RF ablation have been limited, with only a few published case reports (9–12). The purpose of this study was to evaluate the clinical efficacy and safety of embolization in patients with bleeding related to hepatic RF ablation.
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MATERIALS AND METHODS Patient Characteristics and Study Design This study was approved by the institutional review board, and written informed consent for the procedures was obtained from all patients before embolization. A retrospective review was performed for all patients who underwent embolization for bleeding related to hepatic RF ablation between January 2000 and December 2014. The medical records of each patient were reviewed to identify clinical data, such as underlying disease etiology, clinical symptoms or signs, laboratory findings, and clinical outcome after embolization including procedure-related complications. A flow chart for the present study is shown in Figure 1. During the study period, 5,196 patients with 9,743 hepatic tumors underwent 8,303 RF ablation sessions at a single tertiary referral center. Of these patients, 62 (1.2%) experienced bleeding after RF ablation, which was identified on imaging studies performed after ablation procedures. Among these patients, 61 showed direct or indirect signs of hemorrhage on follow-up computed tomography (CT) scans. Indirect signs (46 of 61; 75%) were hemoperitoneum (n ¼ 19; 31%), intrahepatic and subcapsular hematoma (n ¼ 18; 30%), hemothorax (n ¼ 5; 8%), localized hematoma adjacent to the electrode tract (n ¼ 2; 3%), and hemobilia (n ¼ 2; 3%). The direct signs (15 of 61; 25%) were extravasation of contrast media with or without pseudoaneurysm or pseudoaneurysm alone. The remaining 1 patient did not undergo CT scan but hemopericardium was shown on ultrasound (US) performed immediately after RF ablation.
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The final study cohort included 15 patients (12 men and 3 women; mean age 62 y; range, 49–76 y) who underwent embolization for bleeding related to hepatic RF ablation. There were 47 patients excluded; 46 received conservative treatments, including volume replacement with or without transfusion for minimal or transient bleeding without clinical signs (hemodynamic instability or progressive decrease in hemoglobin levels), and 1 patient underwent emergent exploratory thoracotomy for sudden hemodynamic collapse caused by cardiac tamponade. Among the 15 patients in the study cohort, hepatocellular carcinoma was diagnosed in 13 (87%) by at least 2 concordant imaging studies (n ¼ 12) and biopsy (n ¼ 1) based on the guidelines of the American Association for the Study of Liver Disease (13), and metastatic adenocarcinomas from colon cancer (n ¼ 1) and rectal cancer (n ¼ 1) were diagnosed in the remaining 2 (13%) patients. The mean number of tumors was 1.5 (22 nodules; range, 1–3) and the mean size of tumors was 2.3 cm (range, 0.9–5 cm). The locations of hepatic tumors were segment I (n ¼ 1), segment II (n ¼ 2), segment III (n ¼ 1), segment IV (n ¼ 1), segment V (n ¼ 3), segment VI (n ¼ 5), segment VII (n ¼ 1), and segment VIII (n ¼ 9). Table 1 summarizes the characteristics of the study patients.
RF Ablation Procedures The RF ablation procedures were the same as procedures described in previous studies (14,15). The procedures were typically performed percutaneously using US
Figure 1. Flow diagram for study. From January 2000 to December 2014, 5,196 patients with 9,743 tumors underwent 8,303 RF ablation sessions. Of these patients, 62 experienced bleeding after hepatic RF ablation; 15 patients required embolization and composed the final study cohort.
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Table 1 . Characteristics of Study Patients (n ¼ 15)
Month
HCC
1
1.0
II
Dome
CT
12
4
Yes
None
108
11.5/0.98
None
’
2/M/53 3/M/69
HCC HCC
1 1
1.8 1.8
VII VIII
Diaphragm Dome
US CT
12 10
1 2
Yes Yes
Yes (artificial) Yes (artificial)
75 105
19.3/1.73 (13.2/1.20) 11.6/1.02
Yes None
Hepatic Tumor
No.
Nodule
Nodule Location High-Risk
Nodules Size (cm) (Liver Segment)
Image
Ablation
Targeting
Liver
Location* Guidance Time (min) Number† Cirrhosis
Platelets
PT
Ascites
( 103)‡
(s)/INR‡
4/M/66
HCC
3
2.1/1.9/0.9
VIII/V/VI
Capsule
US
10/10/8
1/1/1
Yes
Yes
57
15.4/1.37
None
5/F/68 6/F/63
HCC HCC
2 2
1.5/1.1 3.2/2.9
VIII/VI IV/VIII
HV Capsule
US US
10/10 12/10
2/1 1/1
Yes Yes
None None
99 80
12.6/1.17 12.4/1.14
None None
7/M/54
HCC
1
1.9
VIII/I
IVC
US
12
1
Yes
None
40 (51)
15.3/1.29
Yes
8/M/62 9/M/76
HCC Colon cancer
2 2
2.9/2.3 4.4/2.8
VIII/V VIII/VI
GB PV
US US
12/10 12/10
1/1 1/1
Yes No
None None
66 293
15.0/1.22 12.6/1.03
None None
10/M/62
HCC
1
1.3
VI
Capsule
US
10
1
Yes
None
87
16.3/1.38
None
11/M/49 12/F/57
Rectal cancer HCC
1 1
5.0 2.0
VIII VI
Capsule Capsule
US US
12 10
3 2
No Yes
None None
210 65
10.7/0.91 17.6/1.50
None None
13/M/71
HCC
2
4.0/1.5
V/III
PV
US
12/10
2/1
Yes
None
14/M/69 15/M/62
HCC HCC
1 1
1.1 1.6
VIII II
PV Dome
US US
10 10
1 1
Yes Yes
Yes (artificial) Yes (artificial)
43 (53) 18.9/1.66 (13.1/1.20) 61 79
12.5/1.12 18.1/1.57 (13.7/1.25)
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Coagulopathy
1/M/50
Patient No. /Sex/Age (y)
Yes None Yes
F ¼ female; GB ¼ gallbladder; HCC ¼ hepatocellular carcinoma; HV ¼ hepatic vein; INR ¼ international normalized ratio; IVC ¼ inferior vena cava; M ¼ male; PT ¼ prothrombin time; PV ¼ portal vein. * High-risk location is defined as locations adjacent to the large vessels or extrahepatic organs, hepatic capsule, or hepatic dome (hepatic nodules adjacent to the large vessels were defined as nodules located o 5 mm from the first or second branch of the PV, the base of the HVs, or the IVC, whereas nodules adjacent to the extrahepatic organs were defined as nodules located o 5 mm from the heart, lung, GB, right kidney, gastrointestinal tract, or diaphragm; the hepatic dome is the dead space in a US scan caused by the interfering effect of the lung). † Targeting number is defined as the number of punctures required for proper electrode positioning. ‡ Data in parentheses are corrected values after transfusion therapy (platelet concentrates or fresh-frozen plasma).
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guidance, with moderate sedation and local anesthesia. CT-guided RF ablation was performed in patients with tumors with poor visibility on US. For patients with platelet counts o 50,000/mm3 or international normalized ratio (INR) 4 1.5, transfusion was performed before the procedures. During the procedure, vital signs and cardiac status were monitored by pulse oximetry and electrocardiography. The RF current was emitted for 10–15 minutes using a 200-W generator set (Cool-Tip RF System; Valleylab, Inc, Burlington, Massachusetts) to deliver the maximum power using the automatic impedance control method. The ablation time was subject to the operators’ discretion and based on tumor size, extent of echogenic ablation zone, and patient condition (eg, vital signs, pain). An internally cooled, single or cluster electrode was chosen according to the tumor size. A single electrode with a 2-cm or a 3-cm exposed tip (Valleylab, Inc) was used for tumors r 2 cm in diameter, and a cluster electrode (Valleylab, Inc) or multiple overlapping insertions of a single electrode were used for tumors 4 2 cm in diameter. The endpoint was complete ablation of tumors with margins 4 0.5 cm with the exception of subcapsular and perivascular tumors. In some patients, artificial ascites (n = 220) was created to visualize the lesion or avoid thermal injury to adjacent organs. At the end of the procedure, RF energy of 40–70 W was delivered again before removing the electrode. The electrode path was cauterized while retracting the electrode at a rate of 1 cm/s until the liver capsule to minimize bleeding and tract seeding. A follow-up contrast-enhanced CT scan was performed immediately or 1 day after RF ablation to evaluate the extent of ablation and to identify any possible complications, such as fluid collection or bleeding. The RF ablation procedure was considered to be complete and technically successful if the ablation zone completely covered the tumor and if there was no irregular enhancement. In the case of incomplete ablation, additional RF ablation sessions were planned and performed on the following day, if possible. Patients were discharged from the hospital the day after the procedure if CT images obtained immediately after the procedure or overnight clinical observation showed no complications. Followup contrast-enhanced CT scans were performed 1 month after RF ablation and every 2–3 months thereafter or promptly if there was clinical suspicion of recurrence.
Angiography and Embolization Techniques Common hepatic artery and superior mesenteric artery angiography, along with delayed phase angiography for indirect portography, was performed in patients who showed signs of bleeding on CT scans. In addition, selective angiography was performed to reveal injury to
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the vasculature along the route of electrode insertion, depending on the location of the tumor. In case of active portal bleeding without an arterioportal communication, portography after direct puncture of the portal vein system was performed to demonstrate the culprit portal vein branch with a 5-F angiographic curved catheter (Cobra; Cook, Inc, Bloomington, Indiana) in the main portal vein, with contrast injection at rates of 5–6 mL/s over a period of 4 seconds. Superselection of bleeding vessels was performed using a 2.0-F to 2.4-F microcatheter (Progreat, Terumo Corporation, Tokyo, Japan). Contrast extravasation or the presence of a pseudoaneurysm was considered active bleeding. The suspected abnormalities seen on angiography were matched with abnormalities initially detected on CT scans for confirmation. The vascular abnormalities were treated either by transarterial embolization or by transhepatic portal vein embolization. Embolic materials were chosen according to the operator’s preference based on the angiographic findings and included platinum coils (MicroNester; Cook, Inc), N-butyl cyanoacrylate (Histoacryl; B. Braun Melsungen AG, Melsungen, Germany), and gelatin sponge particles (SPONGOSTAN; Ethicon, Inc, Somerville, New Jersey). N-butyl cyanoacrylate was mixed with iodized oil (Lipiodol; Guerbet, Roissy, France) at a ratio of 1:2. Completion angiography was performed after embolization to confirm target vessel occlusion or cessation of contrast extravasation.
Definitions and Analysis Coagulopathy was defined as an INR of 4 1.5 or a platelet count of o 50,000/mm3 (16). A high-risk location was defined as proximity to large vessels or extrahepatic organs, hepatic capsule, or hepatic dome. Hepatic nodules adjacent to large vessels were defined as nodules located o 5 mm from the first or second branch of the portal vein, the base of hepatic veins, or the inferior vena cava. Nodules adjacent to extrahepatic organs were defined as nodules located o 5 mm from the heart, lung, gallbladder, right kidney, gastrointestinal tract, or diaphragm (17). Technical success was defined as a complete stasis of hemorrhage on angiography performed after embolization. Clinical success was defined as sustained cessation of bleeding with evidence of hemodynamic stability, lack of need for emergency surgery or other interventional procedures within 24 hours, and resolved hemorrhage or pseudoaneurysm on follow-up CT scans. Rebleeding was defined as recurrence of bleeding with a change in vital signs or a decrease in hemoglobin levels of 4 2 g/dL within 1 month after embolization in patients with initial clinical success. Complications were classified as major or minor according to the guidelines of the Society of Interventional Radiology (SIR) Standards of Practice Committee (18).
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RESULTS Clinical Characteristics Four (27%) of 15 patients were referred to the interventional suite because of hemodynamic instability (eg, systemic hypotension, abnormal heart rate, decreased urine outflow), and 11 (73%) patients were referred because of progressively decreasing hemoglobin and hematocrit levels. The present study showed that hepatic nodules related to bleeding after RF ablation were in high-risk locations in all patients: abutting the hepatic capsule (n ¼ 5; 33%), adjacent to large vessels (n ¼ 5; 33% [portal vein, n ¼ 3; base of hepatic vein, n ¼ 1; or inferior vena cava, n ¼ 1]), in the hepatic dome (n ¼ 2; 13%), adjacent to the diaphragm (n ¼ 1; 7%), and near the gallbladder (n ¼ 1; 7%). In 4 patients (27%), artificial ascites (or hydrodissection) was introduced using US guidance to separate the liver and adjacent organs for difficult-to-ablate nodules. Coagulopathy was noted in 4 patients (4 of 15; 27%) showing low platelet counts (o 50,000/mL) or prothrombin time prolongation (INR 41.5), which was corrected through the transfusion of fresh-frozen plasma or platelets before RF ablation. Median INR of all patients was 1.20 (range, 0.91– 1.73), and median platelet count was 138,000/mL (range, 40,000–293,000/mL).
Angiographic Details In all patients, the median time interval between symptom presentation and angiography was 22 hours (mean 38. 4 h; range, 3–168 h). Active bleeding signs, such as contrast extravasation with or without pseudoaneurysm, were seen in all patients. Angiography revealed that 6 patients had hepatic arterial bleeding (segment VIII hepatic artery, n ¼ 4; segment VI hepatic artery, n ¼ 1; segment IV hepatic artery, n ¼ 1) (Fig 2a–d), 1 patient had portal venous bleeding (Fig 3a–f), and 8 patients had extrahepatic arterial bleeding (right posterior intercostal artery, n ¼ 4; right internal thoracic artery, n ¼ 2; right inferior phrenic artery, n ¼ 2) (Figs E1a–d and E2a–d [available online at www.jvir.org]). Among the 15 patients, 14 underwent transarterial embolization, and 1 patient underwent percutaneous transhepatic portal vein embolization. CT and angiographic findings, vessels that received embolization, and embolic materials are summarized in Table 2.
Technical Results and Clinical Outcomes The embolization procedures were technically successful in all patients, and immediate hemostasis was successfully achieved in all 15 patients, resulting in a clinical success rate of 100%. In all study patients, the median transfusion amount before and after angiography was 4 U of packed red blood cells (range, 0–16 U). All patients were discharged alive, and median hospitalization was 8 days (range, 3–48 d). There was no
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rebleeding within 30 days after embolization, and hemorrhage or pseudoaneurysm was resolved on 1-month follow-up CT scans after RF ablation procedures. No embolization-related complications were observed.
DISCUSSION The present study reports a high efficacy of embolization for bleeding complications after hepatic RF ablation, with technical and clinical success rates of 100% and without major complications or mortality. The overall rate of bleeding after hepatic RF ablation was 1.2% in this study—a value that is comparable to other reports (range, 0.32%–1.6%) (9,19–25). Although the incidence of bleeding after hepatic RF ablation is low, bleeding can be fatal (5–8). Thus, prompt detection and appropriate treatment are necessary to avoid serious side effects. Operative management can be a treatment option; however, it is often challenging, especially in patients with comorbidities in whom surgery is contraindicated or in patients with severe hemodynamic instability. Given the availability of minimally invasive techniques, embolization is preferred as the first-line therapeutic option in this clinical setting (9). In this study, although most bleeds (46 of 62; 74%) after RF ablation were minimal and transient and responded well to conservative treatment, close clinical evaluation of patient symptoms, vital signs, and laboratory tests immediately after RF ablation is essential for the early detection and prompt management. Diagnostic angiography is recommended when patients have hemodynamic instability (eg, systemic hypotension, tachycardia, and decreased urine outflow) or show progressively decreasing hemoglobin levels (4 2 g/dL), or when follow-up CT scans demonstrate evidence of bleeding. In a study by Goto et al (19), large tumor size and low platelet count were significant risk factors for hemoperitoneum, and the location of tumor nodule was a significant risk factor for hemothorax and hemobilia. Hemoperitoneum is usually related to mechanical injuries caused by RF ablation electrodes traversing a vessel or thermal injuries sustained during ablation, whereas hemothorax is typically caused by puncturing intercostal or internal thoracic arteries. In the present study, various extrahepatic arterial causes in 8 patients who had been treated with transarterial embolization were demonstrated, which has not been described in previous reports. Knowledge regarding extrahepatic arterial bleeding complications after hepatic RF ablation may allow physicians to detect the culprit vessels on angiography in a timely manner. For instance, right hepatic lobe ablation resulting in hemothorax can direct particular attention to the right intercostal artery during angiography. If intraperitoneal bleeding or anterior chest wall hematoma is seen on a CT scan after ablation to the anterior aspect of the left
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Figure 2. A 74-year-old man underwent RF ablation for hepatic metastasis from rectosigmoid colon cancer. (a) CT image obtained immediately after ablation shows opacification of an irregular intrahepatic pseudoaneurysm (arrow) apart from the ablation site (asterisk) as well as along the course of the needle tract. (b, c) Common hepatic and selective right anterior hepatic angiograms show suspected extravasation of the contrast medium (arrow) along with an arterioportal fistula. (d) The intrahepatic pseudoaneurysm is not noted (arrow) on follow-up CT image obtained 1 week after embolization with gelatin sponge particles.
hepatic lobe, angiography can be used to focus on the internal thoracic arteries. Finally, if intraperitoneal bleeding near the hepatic bare area is observed on CT after tumor ablation in hepatic segment VII adjacent to the diaphragm, angiography can be directed to identify the right inferior phrenic artery. Proximity to the blood vessels, liver capsule, and vital structures is considered to increase the risk for treatment failure and complications (1,17,20,26–30). If a nodule is considered to be at high risk or in a difficult location, we should scrutinize the route of electrode insertion. A percutaneous approach for tumors in high-risk locations is often difficult because of the restrictions of the angle in which the electrode can be inserted caused by the ribs, US interference by the air in the lungs, or suboptimal
positioning of the RF ablation electrode from fear of injuring a vital structure. Previous investigators have demonstrated an increased incidence of complications to classify these tumors as relative contraindications to RF ablation (20,28–31). Once bleeding begins, the possibility of hemostasis depends on platelet function and coagulation activity (16,20). Given that patients with cirrhosis, in particular, are often already in a thrombocytopenic state, the assessment of bleeding risk is important to prevent bleeding complications in RF ablation. Consequently, every effort should be made to correct coagulopathy before and after RF ablation. In most cases, vascular complications, including arterial bleeding, pseudoaneurysm, or arteriovenous fistula,
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Figure 3. A 71-year-old man presented with portal venous bleeding after RF ablation for hepatocellular carcinoma in the right hepatic lobe. (a) CT image obtained 2 hours after RF ablation shows hemorrhagic ascites, with bleeding of the right hepatic surface (arrow) and a wedge-shaped, parenchymal enhancing arterioportal shunt (arrowhead) adjacent to the ablation zone. (b, c) Common hepatic angiogram demonstrates early opacification of the right anteroinferior branch of the portal vein in segment V from the right anteroinferior branch of the hepatic artery supplying segment V (black arrow) (b) and without evidence of active bleeding, which was prophylactically treated using a combination of gelatin sponge particles and 5 microcoils (white arrow) (c). (d) Delayed portogram obtained after embolization reveals contrast medium extravasation from the branch of the right posteroinferior portal vein in segment VI (arrow). (e) Selective portogram via the left portal vein access using the percutaneous transhepatic approach confirms active bleeding (arrow) from the right posteroinferior portal vein branch in segment VI. (f) Active portal venous bleeding is no longer seen after embolization with a combination of gelatin sponge particles, 2 microcoils, and N-butyl cyanoacrylate (arrow).
occur immediately after the procedure. Thus, because of the risk of bleeding, hemodynamic monitoring is recommended for at least 4–6 hours after the procedure (32–34). However, bleeding may often manifest for 4 8 hours, and delayed bleeding after 24 hours occurs rarely. In the present study, the median time interval to angiography was 22 hours (range, 3–168 h). Two patients had late hepatic arterial bleeding after RF ablation, with time intervals of 164 hours and 168 hours, respectively. Kaplan et al (35) demonstrated the mechanism of late hepatic rupture, which is attributed to the breakdown of clot into the hyperosmolar fluid, leading to a greater fluid absorption, increasing the size and pressure within the injured hepatic parenchyma until a breaking point is reached, tearing the tissue and causing bleeding. An additional mechanism—gradual progression of intrahepatic laceration with hematoma from direct penetrating arteriovenous injury—has
been proposed (12). Although most of the blood from an injured hepatic artery passes through the portal vein, some may burrow into the hepatic parenchyma, causing intrahepatic laceration and delayed hepatic rupture. In our cases, delayed hepatic arterial bleeding was treated successfully with transarterial embolization. We report a patient (No. 13) with hemodynamically significant portal venous bleeding who was treated with percutaneous transhepatic portal vein embolization, along with another arterioportal fistula in the nonhemorrhagic segment. In general, portal venous bleeding resolves spontaneously without further intervention because the portal venous system is a system with lower pressure. However, despite conservative treatment, persistent and massive portal venous bleeding can lead to hemodynamic instability, which eventually requires active intervention, as seen in the present study.
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Patient Hb Level No./Sex/ Time Transfusion Age (y) Indication Interval (h)* Before After (pRBCs) CT Findings Angiographic Findings 1/M/50 ↓ Hb 3 9.8 13.3 0 Abdominal wall hematoma, Extravasation, PSA hemoperitoneum 2/M/53 ↓ Hb 4 11.7 13.1 2 Hemoperitoneum Extravasation 3/M/69 ↓ Hb 4 13.2 14.4 1 Abdominal wall hematoma, Extravasation hemoperitoneum 4/M/66 ↓ Hb 60 6.4 10 5 Hemoperitoneum Extravasation 5/F/68 ↓ Hb 164 6 12 10 Hemoperitoneum, Extravasation hemobilia 6/F/63 ↓ Hb 22 7.4 11.4 1 Hemothorax Extravasation 7/M/54 ↓ Hb 48 6.3 10.1 5 Chest wall hematoma, Extravasation, PSA hemoperitoneum 8/M/62 ↓ Hb 31 9 13.2 4 Hemothorax Extravasation 9/M/76 ↓ Hb 22 6.7 11 4 Intrahepatic PSA with APF, Extravasation, APF hemoperitoneum (A8 to PV), PV PSA 10/M/62 ↓ Hb, ↓ BP 72 7.1 10.5 7 Hemothorax, Extravasation, PSA hemoperitoneum 11/M/49 ↓ Hb 10 8.7 14.9 16 Hemoperitoneum Extravasation, PSA 12/F/57 ↓ Hb 22 6.9 11.1 10 Hemoperitoneum Extravasation 13/M/71 ↓ Hb, ↓ BP 5 4.2 7.2 10 Hemoperitoneum Extravasation, APF in nonhemorrhagic segment 14/M/69 ↓ Hb, ↓ BP 71 9.2 14.2 4 Hemoperitoneum Extravasation 15/M/62 ↓ Hb, ↓ BP 168 7 9.5 4 Hemoperitoneum, HA PSA Extravasation, PSA
Embolized Vessels RITA RIPA RICS (10th)
Embolic Material Gelfoam, coil Glue Gelfoam
A6 A8 RITA A8
Technical Clinical Duration of Success Success Complications Hospitalization (d) Yes Yes None 3 Yes Yes
Yes Yes
None None
5 4
Gelfoam Gelfoam
Yes Yes
Yes Yes
None None
8 48
Gelfoam Gelfoam
Yes Yes
Yes Yes
None None
5 6
RICS (6th) Gelfoam, coil A8 Gelfoam
Yes Yes
Yes Yes
None None
9 8
RICS (10th) Gelfoam, coil
Yes
Yes
None
14
A8 RICS (10th) P6
Coil Gelfoam Gelfoam, coil, glue
Yes Yes Yes
Yes Yes Yes
None None None
23 15 36
RIPA A4
Gelfoam Gelfoam
Yes Yes
Yes Yes
None None
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Table 2 . Details of Endovascular Intervention and Outcomes
A4 ¼ hepatic artery supplying segment IV; A5 ¼ hepatic artery supplying segment V; A6 ¼ hepatic artery supplying segment VI; A8 ¼ hepatic artery supplying segment VIII; APF ¼ arterioportal fistula; BP ¼ blood pressure; F ¼ female; HA ¼ hepatic artery; Hb ¼ hemoglobin; M ¼ male; P6 ¼ posteroinferior portal vein branch in segment VI; pRBCs ¼ packed red blood cells; PSA ¼ pseudoaneurysm; RICS ¼ right intercostal artery; RIPA ¼ right inferior phrenic artery; RITA ¼ right internal thoracic artery. * Time interval between symptom presentation and angiography.
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Therefore, patients with life-threatening portal venous bleeding should be emergently treated. This study has some limitations to be considered when interpreting the results. First, there are the inherent limitations posed by the retrospective nature of this study. Second, the number of patients who underwent embolization for bleeding after hepatic RF ablation was relatively small. Because the incidence of bleeding after hepatic RF ablation is not high, this limitation is an innate characteristic of the study, despite the large number of patients who underwent RF ablation. Third, a relative limitation is the lack of a standardized protocol regarding the type of embolic materials and the techniques of embolization. In conclusion, embolization shows a high technical success rate and clinical effectiveness for patients with active bleeding after hepatic RF ablation without the need for surgery. Embolization can be a beneficial option to detect and manage bleeding. Although the incidence of bleeding after hepatic RF ablation is low, the bleeding can be catastrophic. Thus, patients should be closely monitored by clinical and radiologic examinations to allow for early detection of changes that may indicate the development of possible early or delayed bleeding.
ACKNOWLEDGMENTS This study was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Science, ICT and Future Planning (Grant No. 2014R1A2A2A01005857) and the Asan Institute for Life Sciences, Asan Medical Center, Seoul, Korea (Grant No. 16-312). The authors thank So Yeon Kim, MD, and Jonathan K. Park, MD, for assistance with preparation of the manuscript.
REFERENCES 1. de Baere T, Risse O, Kuoch V, et al. Adverse events during radiofrequency treatment of 582 hepatic tumors. AJR Am J Roentgenol 2003; 181:695–700. 2. Curley SA, Marra P, Beaty K, et al. Early and late complications after radiofrequency ablation of malignant liver tumors in 608 patients. Ann Surg 2004; 239:450–458. 3. Tateishi R, Shiina S, Teratani T, et al. Percutaneous radiofrequency ablation for hepatocellular carcinoma. An analysis of 1000 cases. Cancer 2005; 103:1201–1209. 4. Giorgio A, Tarantino L, de Stefano G, Coppola C, Ferraioli G. Complications after percutaneous saline-enhanced radiofrequency ablation of liver tumors: 3-year experience with 336 patients at a single center. AJR Am J Roentgenol 2005; 184:207–211. 5. Mulier S, Mulier P, Ni Y, et al. Complications of radiofrequency coagulation of liver tumours. Br J Surg 2002; 89:1206–1222. 6. Rhim H. Complications of radiofrequency ablation in hepatocellular carcinoma. Abdom Imaging 2005; 30:409–418. 7. Eisele RM, Schumacher G, Jonas S, Neuhaus P. Radiofrequency ablation prior to liver transplantation: focus on complications and on a rare but severe case. Clin Transplant 2008; 22:20–28.
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8. Kong WT, Zhang WW, Qiu YD, et al. Major complications after radiofrequency ablation for liver tumors: analysis of 255 patients. World J Gastroenterol 2009; 15:2651–2656. 9. Carrafiello G, Lagana D, Ianniello A, et al. Bleeding after percutaneous radiofrequency ablation: successful treatment with transcatheter embolization. Eur J Radiol 2007; 61:351–355. 10. Wu XY, Shi XL, Zhou JX, et al. Life-threatening hemorrhage after liver radiofrequency ablation successfully controlled by transarterial embolization. World J Hepatol 2012; 4:419–421. 11. Sonomura T, Kawai N, Kishi K, et al. N-butyl cyanoacrylate embolization with blood flow control of an arterioportal shunt that developed after radiofrequency ablation of hepatocellular carcinoma. Korean J Radiol 2014; 15:250–253. 12. Chang IS, Kim YJ, Park SW, et al. Delayed hepatic rupture after radiofrequency ablation for colorectal hepatic metastasis: management with transcatheter arterial embolization. Ann Surg Treat Res 2014; 87:41–43. 13. Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005; 42:1208–1236. 14. Kim JW, Kim JH, Sung KB, et al. Transarterial chemoembolization vs. radiofrequency ablation for the treatment of single hepatocellular carcinoma 2 cm or smaller. Am J Gastroenterol 2014; 109:1234–1240. 15. Lee CW, Kim JH, Won HJ, et al. Percutaneous radiofrequency ablation of hepatic metastases from gastric adenocarcinoma after gastrectomy. J Vasc Interv Radiol 2015; 26:1172–1179. 16. O’Connor SD, Taylor AJ, Williams EC, Winter TC. Coagulation concepts update. AJR Am J Roentgenol 2009; 193:1656–1664. 17. Teratani T, Yoshida H, Shiina S, et al. Radiofrequency ablation for hepatocellular carcinoma in so-called high-risk locations. Hepatology 2006; 43:1101–1108. 18. Cardella JF, Kundu S, Miller DL, Millward SF, Sacks D. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2009; 20:S189–S191. 19. Goto E, Tateishi R, Shiina S, et al. Hemorrhagic complications of percutaneous radiofrequency ablation for liver tumors. J Clin Gastroenterol 2010; 44:374–380. 20. Livraghi T, Solbiati L, Meloni MF, Gazelle GS, Halpern EF, Goldberg SN. Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study. Radiology 2003; 226:441–451. 21. Rhim H, Dodd GD 3rd, Chintapalli KN, et al. Radiofrequency thermal ablation of abdominal tumors: lessons learned from complications. Radiographics 2004; 24:41–52. 22. Chen MH, Yang W, Yan K, et al. Treatment efficacy of radiofrequency ablation of 338 patients with hepatic malignant tumor and the relevant complications. World J Gastroenterol 2005; 11:6395–6401. 23. Koda M, Murawaki Y, Hirooka Y, et al. Complications of radiofrequency ablation for hepatocellular carcinoma in a multicenter study: an analysis of 16,346 treated nodules in 13,283 patients. Hepatol Res 2012; 42: 1058–1064. 24. Takaki H, Yamakado K, Nakatsuka A, et al. Frequency of and risk factors for complications after liver radiofrequency ablation under CT fluoroscopic guidance in 1500 sessions: single-center experience. AJR Am J Roentgenol 2013; 200:658–664. 25. Kasugai H, Osaki Y, Oka H, Kudo M, Seki T. Severe complications of radiofrequency ablation therapy for hepatocellular carcinoma: an analysis of 3,891 ablations in 2,614 patients. Oncology 2007; 72(suppl 1):72–75. 26. Mulier S, Ni Y, Jamart J, Ruers T, Marchal G, Michel L. Local recurrence after hepatic radiofrequency coagulation: multivariate meta-analysis and review of contributing factors. Ann Surg 2005; 242:158–171. 27. Lu DS, Raman SS, Limanond P, et al. Influence of large peritumoral vessels on outcome of radiofrequency ablation of liver tumors. J Vasc Interv Radiol 2003; 14:1267–1274. 28. Lu DS, Yu NC, Raman SS, et al. Percutaneous radiofrequency ablation of hepatocellular carcinoma as a bridge to liver transplantation. Hepatology 2005; 41:1130–1137. 29. Lencioni R, Cioni D, Crocetti L, et al. Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous imageguided radiofrequency ablation. Radiology 2005; 234:961–967. 30. Sartori S, Tombesi P, Macario F, et al. Subcapsular liver tumors treated with percutaneous radiofrequency ablation: a prospective comparison with nonsubcapsular liver tumors for safety and effectiveness. Radiology 2008; 248:670–679. 31. Llovet JM, Vilana R, Bru C, et al. Increased risk of tumor seeding after percutaneous radiofrequency ablation for single hepatocellular carcinoma. Hepatology 2001; 33:1124–1129.
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32. Rhim H, Dodd GD 3rd. Radiofrequency thermal ablation of liver tumors. J Clin Ultrasound 1999; 27:221–229. 33. Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Solbiati L, Gazelle GS. Small hepatocellular carcinoma: treatment with radiofrequency ablation versus ethanol injection. Radiology 1999; 210: 655–661.
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34. Rossi S, Di Stasi M, Buscarini E, et al. Percutaneous RF interstitial thermal ablation in the treatment of hepatic cancer. AJR Am J Roentgenol 1996; 167:759–768. 35. Kaplan U, Hatoum OA, Chulsky A, Menzal H, Kopelman D. Two weeks delayed bleeding in blunt liver injury: case report and review of the literature. World J Emerg Surg 2011; 6:14.
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Figure E1. A 50-year-old man presented with progressively decreased levels of hemoglobin after RF ablation for hepatocellular carcinoma. (a) CT scan obtained 2 hours after RF ablation shows a pseudoaneurysm (arrow) at an anterior aspect of the ablation site (asterisk) with anterior abdominal hematoma and hemorrhagic ascites along the course of the needle tract. (b, c) Coronal reformatted CT image shows a pseudoaneurysm (arrow) (b) from the branch of the right internal thoracic artery, which was also shown on a right internal thoracic angiogram (arrow) (c). (d) On nonenhanced CT image obtained after embolization, abdominal hematoma and hemorrhagic ascites were nearly resolved after embolization with a combination of gelatin sponge particles and 1 microcoil (arrow) for the right internal thoracic artery.
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Figure E2. A 53-year-old man presented with hemoperitoneum after RF ablation. (a) Enhanced CT image shows a small hepatocellular carcinoma (arrow) in segment VII adjacent to the diaphragm. (b) CT image obtained immediately after ablation shows contrast medium extravasation near the bare area, resulting in hemoperitoneum (arrow). (c) Right inferior phrenic angiogram reveals contrast medium extravasation (arrowheads) from the branches of the right inferior phrenic artery. (d) Right inferior phrenic angiogram after embolization using N-butyl cyanoacrylate demonstrates no further extravasation of the contrast medium.
Embolization for Bleeding after Hepatic Radiofrequency Ablation Jong Woo Kim, MD, Ji Hoon Shin, MD, PhD, Pyo Nyun Kim, MD, PhD, Yong Moon Shin, MD, PhD, Hyung Jin Won, MD, PhD, Gi-Young Ko, MD, PhD, and Hyun-Ki Yoon, MD, PhD
ABSTRACT Purpose: To evaluate safety and clinical efficacy of embolization for management of bleeding after hepatic radiofrequency (RF) ablation. Materials and Methods: From January 2000 to December 2014, 5,196 patients with 9,743 tumors underwent 8,303 RF ablation sessions. Of these patients, 62 experienced bleeding after hepatic RF ablation; 15 patients (12 men and 3 women; mean age 62 y; range, 49–76 y) underwent embolization and composed the final study cohort. Tumors were hepatocellular carcinomas in 13 (87%) patients and metastatic adenocarcinomas from colorectal cancer in 2 (13%) patients. Mean number of tumors was 1.5 (22 nodules; range, 1–3). Tumor locations were segment I (n ¼ 1), segment II (n ¼ 2), segment III (n ¼ 1), segment IV (n ¼ 1), segment V (n ¼ 3), segment VI (n ¼ 5), segment VII (n ¼ 1), and segment VIII (n ¼ 9). Mean tumor size was 2.3 cm (range, 0.9–5 cm). Results: Median time interval between presentation and angiography was 22 hours (mean 38.4 h; range, 3–168 h). On angiography, contrast extravasation with or without pseudoaneurysm was seen in all 15 patients; 14 patients underwent transarterial embolization, and 1 patient underwent percutaneous transhepatic portal vein embolization. Successful hemostasis was achieved in all patients. There was no rebleeding within 30 days after embolization. No embolization-related major complications were observed. Conclusions: Embolization is safe and effective for controlling bleeding related to hepatic RF ablation without the need for surgery.
ABBREVIATION INR = international normalized ratio
Radiofrequency (RF) ablation is considered a relatively safe and minimally invasive treatment for primary and secondary hepatic neoplasms. However, it has been shown to be associated with various complications.
From the Department of Radiology (J.W.K.), Gachon University Gil Medical Center, Incheon, Korea; and Department of Radiology and Research Institute of Radiology (J.W.K., J.H.S., P.N.K., Y.M.S., H.J.W., G.-Y.K., H.-K.Y.), University of Ulsan College of Medicine, Asan Medical Center, 88, Olympic-Ro 43-Gil, Songpa-Gu, Seoul 05505, Korea. Received February 16, 2016; final revision received September 28, 2016; accepted September 29, 2016. Address correspondence to J.H.S.; E-mail: [email protected] None of the authors have identified a conflict of interest. Figures E1 and E2 are available online at www.jvir.org. & SIR, 2016 J Vasc Interv Radiol 2016; XX:]]]–]]] http://dx.doi.org/10.1016/j.jvir.2016.09.031
The estimated range of mortality rates is 0.1%–0.5%, and the estimated range of major complications is 2.2%– 3.1% (1–4). In particular, among the major adverse outcomes of RF ablation, bleeding complications, such as hemobilia, hemoperitoneum, and hemothorax, can be life-threatening if diagnosis and treatment are delayed (5–8). Thus, prompt management of such bleeding complications is essential for successful treatment using RF ablation. Embolization has been shown to have advantages over surgery for the management of bleeding complications related to RF ablation (9). However, to the best of our knowledge, reports focusing on embolization for active bleeding after hepatic RF ablation have been limited, with only a few published case reports (9–12). The purpose of this study was to evaluate the clinical efficacy and safety of embolization in patients with bleeding related to hepatic RF ablation.
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MATERIALS AND METHODS Patient Characteristics and Study Design This study was approved by the institutional review board, and written informed consent for the procedures was obtained from all patients before embolization. A retrospective review was performed for all patients who underwent embolization for bleeding related to hepatic RF ablation between January 2000 and December 2014. The medical records of each patient were reviewed to identify clinical data, such as underlying disease etiology, clinical symptoms or signs, laboratory findings, and clinical outcome after embolization including procedure-related complications. A flow chart for the present study is shown in Figure 1. During the study period, 5,196 patients with 9,743 hepatic tumors underwent 8,303 RF ablation sessions at a single tertiary referral center. Of these patients, 62 (1.2%) experienced bleeding after RF ablation, which was identified on imaging studies performed after ablation procedures. Among these patients, 61 showed direct or indirect signs of hemorrhage on follow-up computed tomography (CT) scans. Indirect signs (46 of 61; 75%) were hemoperitoneum (n ¼ 19; 31%), intrahepatic and subcapsular hematoma (n ¼ 18; 30%), hemothorax (n ¼ 5; 8%), localized hematoma adjacent to the electrode tract (n ¼ 2; 3%), and hemobilia (n ¼ 2; 3%). The direct signs (15 of 61; 25%) were extravasation of contrast media with or without pseudoaneurysm or pseudoaneurysm alone. The remaining 1 patient did not undergo CT scan but hemopericardium was shown on ultrasound (US) performed immediately after RF ablation.
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The final study cohort included 15 patients (12 men and 3 women; mean age 62 y; range, 49–76 y) who underwent embolization for bleeding related to hepatic RF ablation. There were 47 patients excluded; 46 received conservative treatments, including volume replacement with or without transfusion for minimal or transient bleeding without clinical signs (hemodynamic instability or progressive decrease in hemoglobin levels), and 1 patient underwent emergent exploratory thoracotomy for sudden hemodynamic collapse caused by cardiac tamponade. Among the 15 patients in the study cohort, hepatocellular carcinoma was diagnosed in 13 (87%) by at least 2 concordant imaging studies (n ¼ 12) and biopsy (n ¼ 1) based on the guidelines of the American Association for the Study of Liver Disease (13), and metastatic adenocarcinomas from colon cancer (n ¼ 1) and rectal cancer (n ¼ 1) were diagnosed in the remaining 2 (13%) patients. The mean number of tumors was 1.5 (22 nodules; range, 1–3) and the mean size of tumors was 2.3 cm (range, 0.9–5 cm). The locations of hepatic tumors were segment I (n ¼ 1), segment II (n ¼ 2), segment III (n ¼ 1), segment IV (n ¼ 1), segment V (n ¼ 3), segment VI (n ¼ 5), segment VII (n ¼ 1), and segment VIII (n ¼ 9). Table 1 summarizes the characteristics of the study patients.
RF Ablation Procedures The RF ablation procedures were the same as procedures described in previous studies (14,15). The procedures were typically performed percutaneously using US
Figure 1. Flow diagram for study. From January 2000 to December 2014, 5,196 patients with 9,743 tumors underwent 8,303 RF ablation sessions. Of these patients, 62 experienced bleeding after hepatic RF ablation; 15 patients required embolization and composed the final study cohort.
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Table 1 . Characteristics of Study Patients (n ¼ 15)
Month
HCC
1
1.0
II
Dome
CT
12
4
Yes
None
108
11.5/0.98
None
’
2/M/53 3/M/69
HCC HCC
1 1
1.8 1.8
VII VIII
Diaphragm Dome
US CT
12 10
1 2
Yes Yes
Yes (artificial) Yes (artificial)
75 105
19.3/1.73 (13.2/1.20) 11.6/1.02
Yes None
Hepatic Tumor
No.
Nodule
Nodule Location High-Risk
Nodules Size (cm) (Liver Segment)
Image
Ablation
Targeting
Liver
Location* Guidance Time (min) Number† Cirrhosis
Platelets
PT
Ascites
( 103)‡
(s)/INR‡
4/M/66
HCC
3
2.1/1.9/0.9
VIII/V/VI
Capsule
US
10/10/8
1/1/1
Yes
Yes
57
15.4/1.37
None
5/F/68 6/F/63
HCC HCC
2 2
1.5/1.1 3.2/2.9
VIII/VI IV/VIII
HV Capsule
US US
10/10 12/10
2/1 1/1
Yes Yes
None None
99 80
12.6/1.17 12.4/1.14
None None
7/M/54
HCC
1
1.9
VIII/I
IVC
US
12
1
Yes
None
40 (51)
15.3/1.29
Yes
8/M/62 9/M/76
HCC Colon cancer
2 2
2.9/2.3 4.4/2.8
VIII/V VIII/VI
GB PV
US US
12/10 12/10
1/1 1/1
Yes No
None None
66 293
15.0/1.22 12.6/1.03
None None
10/M/62
HCC
1
1.3
VI
Capsule
US
10
1
Yes
None
87
16.3/1.38
None
11/M/49 12/F/57
Rectal cancer HCC
1 1
5.0 2.0
VIII VI
Capsule Capsule
US US
12 10
3 2
No Yes
None None
210 65
10.7/0.91 17.6/1.50
None None
13/M/71
HCC
2
4.0/1.5
V/III
PV
US
12/10
2/1
Yes
None
14/M/69 15/M/62
HCC HCC
1 1
1.1 1.6
VIII II
PV Dome
US US
10 10
1 1
Yes Yes
Yes (artificial) Yes (artificial)
43 (53) 18.9/1.66 (13.1/1.20) 61 79
12.5/1.12 18.1/1.57 (13.7/1.25)
2016
Coagulopathy
1/M/50
Patient No. /Sex/Age (y)
Yes None Yes
F ¼ female; GB ¼ gallbladder; HCC ¼ hepatocellular carcinoma; HV ¼ hepatic vein; INR ¼ international normalized ratio; IVC ¼ inferior vena cava; M ¼ male; PT ¼ prothrombin time; PV ¼ portal vein. * High-risk location is defined as locations adjacent to the large vessels or extrahepatic organs, hepatic capsule, or hepatic dome (hepatic nodules adjacent to the large vessels were defined as nodules located o 5 mm from the first or second branch of the PV, the base of the HVs, or the IVC, whereas nodules adjacent to the extrahepatic organs were defined as nodules located o 5 mm from the heart, lung, GB, right kidney, gastrointestinal tract, or diaphragm; the hepatic dome is the dead space in a US scan caused by the interfering effect of the lung). † Targeting number is defined as the number of punctures required for proper electrode positioning. ‡ Data in parentheses are corrected values after transfusion therapy (platelet concentrates or fresh-frozen plasma).
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guidance, with moderate sedation and local anesthesia. CT-guided RF ablation was performed in patients with tumors with poor visibility on US. For patients with platelet counts o 50,000/mm3 or international normalized ratio (INR) 4 1.5, transfusion was performed before the procedures. During the procedure, vital signs and cardiac status were monitored by pulse oximetry and electrocardiography. The RF current was emitted for 10–15 minutes using a 200-W generator set (Cool-Tip RF System; Valleylab, Inc, Burlington, Massachusetts) to deliver the maximum power using the automatic impedance control method. The ablation time was subject to the operators’ discretion and based on tumor size, extent of echogenic ablation zone, and patient condition (eg, vital signs, pain). An internally cooled, single or cluster electrode was chosen according to the tumor size. A single electrode with a 2-cm or a 3-cm exposed tip (Valleylab, Inc) was used for tumors r 2 cm in diameter, and a cluster electrode (Valleylab, Inc) or multiple overlapping insertions of a single electrode were used for tumors 4 2 cm in diameter. The endpoint was complete ablation of tumors with margins 4 0.5 cm with the exception of subcapsular and perivascular tumors. In some patients, artificial ascites (n = 220) was created to visualize the lesion or avoid thermal injury to adjacent organs. At the end of the procedure, RF energy of 40–70 W was delivered again before removing the electrode. The electrode path was cauterized while retracting the electrode at a rate of 1 cm/s until the liver capsule to minimize bleeding and tract seeding. A follow-up contrast-enhanced CT scan was performed immediately or 1 day after RF ablation to evaluate the extent of ablation and to identify any possible complications, such as fluid collection or bleeding. The RF ablation procedure was considered to be complete and technically successful if the ablation zone completely covered the tumor and if there was no irregular enhancement. In the case of incomplete ablation, additional RF ablation sessions were planned and performed on the following day, if possible. Patients were discharged from the hospital the day after the procedure if CT images obtained immediately after the procedure or overnight clinical observation showed no complications. Followup contrast-enhanced CT scans were performed 1 month after RF ablation and every 2–3 months thereafter or promptly if there was clinical suspicion of recurrence.
Angiography and Embolization Techniques Common hepatic artery and superior mesenteric artery angiography, along with delayed phase angiography for indirect portography, was performed in patients who showed signs of bleeding on CT scans. In addition, selective angiography was performed to reveal injury to
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the vasculature along the route of electrode insertion, depending on the location of the tumor. In case of active portal bleeding without an arterioportal communication, portography after direct puncture of the portal vein system was performed to demonstrate the culprit portal vein branch with a 5-F angiographic curved catheter (Cobra; Cook, Inc, Bloomington, Indiana) in the main portal vein, with contrast injection at rates of 5–6 mL/s over a period of 4 seconds. Superselection of bleeding vessels was performed using a 2.0-F to 2.4-F microcatheter (Progreat, Terumo Corporation, Tokyo, Japan). Contrast extravasation or the presence of a pseudoaneurysm was considered active bleeding. The suspected abnormalities seen on angiography were matched with abnormalities initially detected on CT scans for confirmation. The vascular abnormalities were treated either by transarterial embolization or by transhepatic portal vein embolization. Embolic materials were chosen according to the operator’s preference based on the angiographic findings and included platinum coils (MicroNester; Cook, Inc), N-butyl cyanoacrylate (Histoacryl; B. Braun Melsungen AG, Melsungen, Germany), and gelatin sponge particles (SPONGOSTAN; Ethicon, Inc, Somerville, New Jersey). N-butyl cyanoacrylate was mixed with iodized oil (Lipiodol; Guerbet, Roissy, France) at a ratio of 1:2. Completion angiography was performed after embolization to confirm target vessel occlusion or cessation of contrast extravasation.
Definitions and Analysis Coagulopathy was defined as an INR of 4 1.5 or a platelet count of o 50,000/mm3 (16). A high-risk location was defined as proximity to large vessels or extrahepatic organs, hepatic capsule, or hepatic dome. Hepatic nodules adjacent to large vessels were defined as nodules located o 5 mm from the first or second branch of the portal vein, the base of hepatic veins, or the inferior vena cava. Nodules adjacent to extrahepatic organs were defined as nodules located o 5 mm from the heart, lung, gallbladder, right kidney, gastrointestinal tract, or diaphragm (17). Technical success was defined as a complete stasis of hemorrhage on angiography performed after embolization. Clinical success was defined as sustained cessation of bleeding with evidence of hemodynamic stability, lack of need for emergency surgery or other interventional procedures within 24 hours, and resolved hemorrhage or pseudoaneurysm on follow-up CT scans. Rebleeding was defined as recurrence of bleeding with a change in vital signs or a decrease in hemoglobin levels of 4 2 g/dL within 1 month after embolization in patients with initial clinical success. Complications were classified as major or minor according to the guidelines of the Society of Interventional Radiology (SIR) Standards of Practice Committee (18).
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RESULTS Clinical Characteristics Four (27%) of 15 patients were referred to the interventional suite because of hemodynamic instability (eg, systemic hypotension, abnormal heart rate, decreased urine outflow), and 11 (73%) patients were referred because of progressively decreasing hemoglobin and hematocrit levels. The present study showed that hepatic nodules related to bleeding after RF ablation were in high-risk locations in all patients: abutting the hepatic capsule (n ¼ 5; 33%), adjacent to large vessels (n ¼ 5; 33% [portal vein, n ¼ 3; base of hepatic vein, n ¼ 1; or inferior vena cava, n ¼ 1]), in the hepatic dome (n ¼ 2; 13%), adjacent to the diaphragm (n ¼ 1; 7%), and near the gallbladder (n ¼ 1; 7%). In 4 patients (27%), artificial ascites (or hydrodissection) was introduced using US guidance to separate the liver and adjacent organs for difficult-to-ablate nodules. Coagulopathy was noted in 4 patients (4 of 15; 27%) showing low platelet counts (o 50,000/mL) or prothrombin time prolongation (INR 41.5), which was corrected through the transfusion of fresh-frozen plasma or platelets before RF ablation. Median INR of all patients was 1.20 (range, 0.91– 1.73), and median platelet count was 138,000/mL (range, 40,000–293,000/mL).
Angiographic Details In all patients, the median time interval between symptom presentation and angiography was 22 hours (mean 38. 4 h; range, 3–168 h). Active bleeding signs, such as contrast extravasation with or without pseudoaneurysm, were seen in all patients. Angiography revealed that 6 patients had hepatic arterial bleeding (segment VIII hepatic artery, n ¼ 4; segment VI hepatic artery, n ¼ 1; segment IV hepatic artery, n ¼ 1) (Fig 2a–d), 1 patient had portal venous bleeding (Fig 3a–f), and 8 patients had extrahepatic arterial bleeding (right posterior intercostal artery, n ¼ 4; right internal thoracic artery, n ¼ 2; right inferior phrenic artery, n ¼ 2) (Figs E1a–d and E2a–d [available online at www.jvir.org]). Among the 15 patients, 14 underwent transarterial embolization, and 1 patient underwent percutaneous transhepatic portal vein embolization. CT and angiographic findings, vessels that received embolization, and embolic materials are summarized in Table 2.
Technical Results and Clinical Outcomes The embolization procedures were technically successful in all patients, and immediate hemostasis was successfully achieved in all 15 patients, resulting in a clinical success rate of 100%. In all study patients, the median transfusion amount before and after angiography was 4 U of packed red blood cells (range, 0–16 U). All patients were discharged alive, and median hospitalization was 8 days (range, 3–48 d). There was no
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rebleeding within 30 days after embolization, and hemorrhage or pseudoaneurysm was resolved on 1-month follow-up CT scans after RF ablation procedures. No embolization-related complications were observed.
DISCUSSION The present study reports a high efficacy of embolization for bleeding complications after hepatic RF ablation, with technical and clinical success rates of 100% and without major complications or mortality. The overall rate of bleeding after hepatic RF ablation was 1.2% in this study—a value that is comparable to other reports (range, 0.32%–1.6%) (9,19–25). Although the incidence of bleeding after hepatic RF ablation is low, bleeding can be fatal (5–8). Thus, prompt detection and appropriate treatment are necessary to avoid serious side effects. Operative management can be a treatment option; however, it is often challenging, especially in patients with comorbidities in whom surgery is contraindicated or in patients with severe hemodynamic instability. Given the availability of minimally invasive techniques, embolization is preferred as the first-line therapeutic option in this clinical setting (9). In this study, although most bleeds (46 of 62; 74%) after RF ablation were minimal and transient and responded well to conservative treatment, close clinical evaluation of patient symptoms, vital signs, and laboratory tests immediately after RF ablation is essential for the early detection and prompt management. Diagnostic angiography is recommended when patients have hemodynamic instability (eg, systemic hypotension, tachycardia, and decreased urine outflow) or show progressively decreasing hemoglobin levels (4 2 g/dL), or when follow-up CT scans demonstrate evidence of bleeding. In a study by Goto et al (19), large tumor size and low platelet count were significant risk factors for hemoperitoneum, and the location of tumor nodule was a significant risk factor for hemothorax and hemobilia. Hemoperitoneum is usually related to mechanical injuries caused by RF ablation electrodes traversing a vessel or thermal injuries sustained during ablation, whereas hemothorax is typically caused by puncturing intercostal or internal thoracic arteries. In the present study, various extrahepatic arterial causes in 8 patients who had been treated with transarterial embolization were demonstrated, which has not been described in previous reports. Knowledge regarding extrahepatic arterial bleeding complications after hepatic RF ablation may allow physicians to detect the culprit vessels on angiography in a timely manner. For instance, right hepatic lobe ablation resulting in hemothorax can direct particular attention to the right intercostal artery during angiography. If intraperitoneal bleeding or anterior chest wall hematoma is seen on a CT scan after ablation to the anterior aspect of the left
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Figure 2. A 74-year-old man underwent RF ablation for hepatic metastasis from rectosigmoid colon cancer. (a) CT image obtained immediately after ablation shows opacification of an irregular intrahepatic pseudoaneurysm (arrow) apart from the ablation site (asterisk) as well as along the course of the needle tract. (b, c) Common hepatic and selective right anterior hepatic angiograms show suspected extravasation of the contrast medium (arrow) along with an arterioportal fistula. (d) The intrahepatic pseudoaneurysm is not noted (arrow) on follow-up CT image obtained 1 week after embolization with gelatin sponge particles.
hepatic lobe, angiography can be used to focus on the internal thoracic arteries. Finally, if intraperitoneal bleeding near the hepatic bare area is observed on CT after tumor ablation in hepatic segment VII adjacent to the diaphragm, angiography can be directed to identify the right inferior phrenic artery. Proximity to the blood vessels, liver capsule, and vital structures is considered to increase the risk for treatment failure and complications (1,17,20,26–30). If a nodule is considered to be at high risk or in a difficult location, we should scrutinize the route of electrode insertion. A percutaneous approach for tumors in high-risk locations is often difficult because of the restrictions of the angle in which the electrode can be inserted caused by the ribs, US interference by the air in the lungs, or suboptimal
positioning of the RF ablation electrode from fear of injuring a vital structure. Previous investigators have demonstrated an increased incidence of complications to classify these tumors as relative contraindications to RF ablation (20,28–31). Once bleeding begins, the possibility of hemostasis depends on platelet function and coagulation activity (16,20). Given that patients with cirrhosis, in particular, are often already in a thrombocytopenic state, the assessment of bleeding risk is important to prevent bleeding complications in RF ablation. Consequently, every effort should be made to correct coagulopathy before and after RF ablation. In most cases, vascular complications, including arterial bleeding, pseudoaneurysm, or arteriovenous fistula,
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Figure 3. A 71-year-old man presented with portal venous bleeding after RF ablation for hepatocellular carcinoma in the right hepatic lobe. (a) CT image obtained 2 hours after RF ablation shows hemorrhagic ascites, with bleeding of the right hepatic surface (arrow) and a wedge-shaped, parenchymal enhancing arterioportal shunt (arrowhead) adjacent to the ablation zone. (b, c) Common hepatic angiogram demonstrates early opacification of the right anteroinferior branch of the portal vein in segment V from the right anteroinferior branch of the hepatic artery supplying segment V (black arrow) (b) and without evidence of active bleeding, which was prophylactically treated using a combination of gelatin sponge particles and 5 microcoils (white arrow) (c). (d) Delayed portogram obtained after embolization reveals contrast medium extravasation from the branch of the right posteroinferior portal vein in segment VI (arrow). (e) Selective portogram via the left portal vein access using the percutaneous transhepatic approach confirms active bleeding (arrow) from the right posteroinferior portal vein branch in segment VI. (f) Active portal venous bleeding is no longer seen after embolization with a combination of gelatin sponge particles, 2 microcoils, and N-butyl cyanoacrylate (arrow).
occur immediately after the procedure. Thus, because of the risk of bleeding, hemodynamic monitoring is recommended for at least 4–6 hours after the procedure (32–34). However, bleeding may often manifest for 4 8 hours, and delayed bleeding after 24 hours occurs rarely. In the present study, the median time interval to angiography was 22 hours (range, 3–168 h). Two patients had late hepatic arterial bleeding after RF ablation, with time intervals of 164 hours and 168 hours, respectively. Kaplan et al (35) demonstrated the mechanism of late hepatic rupture, which is attributed to the breakdown of clot into the hyperosmolar fluid, leading to a greater fluid absorption, increasing the size and pressure within the injured hepatic parenchyma until a breaking point is reached, tearing the tissue and causing bleeding. An additional mechanism—gradual progression of intrahepatic laceration with hematoma from direct penetrating arteriovenous injury—has
been proposed (12). Although most of the blood from an injured hepatic artery passes through the portal vein, some may burrow into the hepatic parenchyma, causing intrahepatic laceration and delayed hepatic rupture. In our cases, delayed hepatic arterial bleeding was treated successfully with transarterial embolization. We report a patient (No. 13) with hemodynamically significant portal venous bleeding who was treated with percutaneous transhepatic portal vein embolization, along with another arterioportal fistula in the nonhemorrhagic segment. In general, portal venous bleeding resolves spontaneously without further intervention because the portal venous system is a system with lower pressure. However, despite conservative treatment, persistent and massive portal venous bleeding can lead to hemodynamic instability, which eventually requires active intervention, as seen in the present study.
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Patient Hb Level No./Sex/ Time Transfusion Age (y) Indication Interval (h)* Before After (pRBCs) CT Findings Angiographic Findings 1/M/50 ↓ Hb 3 9.8 13.3 0 Abdominal wall hematoma, Extravasation, PSA hemoperitoneum 2/M/53 ↓ Hb 4 11.7 13.1 2 Hemoperitoneum Extravasation 3/M/69 ↓ Hb 4 13.2 14.4 1 Abdominal wall hematoma, Extravasation hemoperitoneum 4/M/66 ↓ Hb 60 6.4 10 5 Hemoperitoneum Extravasation 5/F/68 ↓ Hb 164 6 12 10 Hemoperitoneum, Extravasation hemobilia 6/F/63 ↓ Hb 22 7.4 11.4 1 Hemothorax Extravasation 7/M/54 ↓ Hb 48 6.3 10.1 5 Chest wall hematoma, Extravasation, PSA hemoperitoneum 8/M/62 ↓ Hb 31 9 13.2 4 Hemothorax Extravasation 9/M/76 ↓ Hb 22 6.7 11 4 Intrahepatic PSA with APF, Extravasation, APF hemoperitoneum (A8 to PV), PV PSA 10/M/62 ↓ Hb, ↓ BP 72 7.1 10.5 7 Hemothorax, Extravasation, PSA hemoperitoneum 11/M/49 ↓ Hb 10 8.7 14.9 16 Hemoperitoneum Extravasation, PSA 12/F/57 ↓ Hb 22 6.9 11.1 10 Hemoperitoneum Extravasation 13/M/71 ↓ Hb, ↓ BP 5 4.2 7.2 10 Hemoperitoneum Extravasation, APF in nonhemorrhagic segment 14/M/69 ↓ Hb, ↓ BP 71 9.2 14.2 4 Hemoperitoneum Extravasation 15/M/62 ↓ Hb, ↓ BP 168 7 9.5 4 Hemoperitoneum, HA PSA Extravasation, PSA
Embolized Vessels RITA RIPA RICS (10th)
Embolic Material Gelfoam, coil Glue Gelfoam
A6 A8 RITA A8
Technical Clinical Duration of Success Success Complications Hospitalization (d) Yes Yes None 3 Yes Yes
Yes Yes
None None
5 4
Gelfoam Gelfoam
Yes Yes
Yes Yes
None None
8 48
Gelfoam Gelfoam
Yes Yes
Yes Yes
None None
5 6
RICS (6th) Gelfoam, coil A8 Gelfoam
Yes Yes
Yes Yes
None None
9 8
RICS (10th) Gelfoam, coil
Yes
Yes
None
14
A8 RICS (10th) P6
Coil Gelfoam Gelfoam, coil, glue
Yes Yes Yes
Yes Yes Yes
None None None
23 15 36
RIPA A4
Gelfoam Gelfoam
Yes Yes
Yes Yes
None None
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Table 2 . Details of Endovascular Intervention and Outcomes
A4 ¼ hepatic artery supplying segment IV; A5 ¼ hepatic artery supplying segment V; A6 ¼ hepatic artery supplying segment VI; A8 ¼ hepatic artery supplying segment VIII; APF ¼ arterioportal fistula; BP ¼ blood pressure; F ¼ female; HA ¼ hepatic artery; Hb ¼ hemoglobin; M ¼ male; P6 ¼ posteroinferior portal vein branch in segment VI; pRBCs ¼ packed red blood cells; PSA ¼ pseudoaneurysm; RICS ¼ right intercostal artery; RIPA ¼ right inferior phrenic artery; RITA ¼ right internal thoracic artery. * Time interval between symptom presentation and angiography.
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Therefore, patients with life-threatening portal venous bleeding should be emergently treated. This study has some limitations to be considered when interpreting the results. First, there are the inherent limitations posed by the retrospective nature of this study. Second, the number of patients who underwent embolization for bleeding after hepatic RF ablation was relatively small. Because the incidence of bleeding after hepatic RF ablation is not high, this limitation is an innate characteristic of the study, despite the large number of patients who underwent RF ablation. Third, a relative limitation is the lack of a standardized protocol regarding the type of embolic materials and the techniques of embolization. In conclusion, embolization shows a high technical success rate and clinical effectiveness for patients with active bleeding after hepatic RF ablation without the need for surgery. Embolization can be a beneficial option to detect and manage bleeding. Although the incidence of bleeding after hepatic RF ablation is low, the bleeding can be catastrophic. Thus, patients should be closely monitored by clinical and radiologic examinations to allow for early detection of changes that may indicate the development of possible early or delayed bleeding.
ACKNOWLEDGMENTS This study was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Science, ICT and Future Planning (Grant No. 2014R1A2A2A01005857) and the Asan Institute for Life Sciences, Asan Medical Center, Seoul, Korea (Grant No. 16-312). The authors thank So Yeon Kim, MD, and Jonathan K. Park, MD, for assistance with preparation of the manuscript.
REFERENCES 1. de Baere T, Risse O, Kuoch V, et al. Adverse events during radiofrequency treatment of 582 hepatic tumors. AJR Am J Roentgenol 2003; 181:695–700. 2. Curley SA, Marra P, Beaty K, et al. Early and late complications after radiofrequency ablation of malignant liver tumors in 608 patients. Ann Surg 2004; 239:450–458. 3. Tateishi R, Shiina S, Teratani T, et al. Percutaneous radiofrequency ablation for hepatocellular carcinoma. An analysis of 1000 cases. Cancer 2005; 103:1201–1209. 4. Giorgio A, Tarantino L, de Stefano G, Coppola C, Ferraioli G. Complications after percutaneous saline-enhanced radiofrequency ablation of liver tumors: 3-year experience with 336 patients at a single center. AJR Am J Roentgenol 2005; 184:207–211. 5. Mulier S, Mulier P, Ni Y, et al. Complications of radiofrequency coagulation of liver tumours. Br J Surg 2002; 89:1206–1222. 6. Rhim H. Complications of radiofrequency ablation in hepatocellular carcinoma. Abdom Imaging 2005; 30:409–418. 7. Eisele RM, Schumacher G, Jonas S, Neuhaus P. Radiofrequency ablation prior to liver transplantation: focus on complications and on a rare but severe case. Clin Transplant 2008; 22:20–28.
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8. Kong WT, Zhang WW, Qiu YD, et al. Major complications after radiofrequency ablation for liver tumors: analysis of 255 patients. World J Gastroenterol 2009; 15:2651–2656. 9. Carrafiello G, Lagana D, Ianniello A, et al. Bleeding after percutaneous radiofrequency ablation: successful treatment with transcatheter embolization. Eur J Radiol 2007; 61:351–355. 10. Wu XY, Shi XL, Zhou JX, et al. Life-threatening hemorrhage after liver radiofrequency ablation successfully controlled by transarterial embolization. World J Hepatol 2012; 4:419–421. 11. Sonomura T, Kawai N, Kishi K, et al. N-butyl cyanoacrylate embolization with blood flow control of an arterioportal shunt that developed after radiofrequency ablation of hepatocellular carcinoma. Korean J Radiol 2014; 15:250–253. 12. Chang IS, Kim YJ, Park SW, et al. Delayed hepatic rupture after radiofrequency ablation for colorectal hepatic metastasis: management with transcatheter arterial embolization. Ann Surg Treat Res 2014; 87:41–43. 13. Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005; 42:1208–1236. 14. Kim JW, Kim JH, Sung KB, et al. Transarterial chemoembolization vs. radiofrequency ablation for the treatment of single hepatocellular carcinoma 2 cm or smaller. Am J Gastroenterol 2014; 109:1234–1240. 15. Lee CW, Kim JH, Won HJ, et al. Percutaneous radiofrequency ablation of hepatic metastases from gastric adenocarcinoma after gastrectomy. J Vasc Interv Radiol 2015; 26:1172–1179. 16. O’Connor SD, Taylor AJ, Williams EC, Winter TC. Coagulation concepts update. AJR Am J Roentgenol 2009; 193:1656–1664. 17. Teratani T, Yoshida H, Shiina S, et al. Radiofrequency ablation for hepatocellular carcinoma in so-called high-risk locations. Hepatology 2006; 43:1101–1108. 18. Cardella JF, Kundu S, Miller DL, Millward SF, Sacks D. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2009; 20:S189–S191. 19. Goto E, Tateishi R, Shiina S, et al. Hemorrhagic complications of percutaneous radiofrequency ablation for liver tumors. J Clin Gastroenterol 2010; 44:374–380. 20. Livraghi T, Solbiati L, Meloni MF, Gazelle GS, Halpern EF, Goldberg SN. Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study. Radiology 2003; 226:441–451. 21. Rhim H, Dodd GD 3rd, Chintapalli KN, et al. Radiofrequency thermal ablation of abdominal tumors: lessons learned from complications. Radiographics 2004; 24:41–52. 22. Chen MH, Yang W, Yan K, et al. Treatment efficacy of radiofrequency ablation of 338 patients with hepatic malignant tumor and the relevant complications. World J Gastroenterol 2005; 11:6395–6401. 23. Koda M, Murawaki Y, Hirooka Y, et al. Complications of radiofrequency ablation for hepatocellular carcinoma in a multicenter study: an analysis of 16,346 treated nodules in 13,283 patients. Hepatol Res 2012; 42: 1058–1064. 24. Takaki H, Yamakado K, Nakatsuka A, et al. Frequency of and risk factors for complications after liver radiofrequency ablation under CT fluoroscopic guidance in 1500 sessions: single-center experience. AJR Am J Roentgenol 2013; 200:658–664. 25. Kasugai H, Osaki Y, Oka H, Kudo M, Seki T. Severe complications of radiofrequency ablation therapy for hepatocellular carcinoma: an analysis of 3,891 ablations in 2,614 patients. Oncology 2007; 72(suppl 1):72–75. 26. Mulier S, Ni Y, Jamart J, Ruers T, Marchal G, Michel L. Local recurrence after hepatic radiofrequency coagulation: multivariate meta-analysis and review of contributing factors. Ann Surg 2005; 242:158–171. 27. Lu DS, Raman SS, Limanond P, et al. Influence of large peritumoral vessels on outcome of radiofrequency ablation of liver tumors. J Vasc Interv Radiol 2003; 14:1267–1274. 28. Lu DS, Yu NC, Raman SS, et al. Percutaneous radiofrequency ablation of hepatocellular carcinoma as a bridge to liver transplantation. Hepatology 2005; 41:1130–1137. 29. Lencioni R, Cioni D, Crocetti L, et al. Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous imageguided radiofrequency ablation. Radiology 2005; 234:961–967. 30. Sartori S, Tombesi P, Macario F, et al. Subcapsular liver tumors treated with percutaneous radiofrequency ablation: a prospective comparison with nonsubcapsular liver tumors for safety and effectiveness. Radiology 2008; 248:670–679. 31. Llovet JM, Vilana R, Bru C, et al. Increased risk of tumor seeding after percutaneous radiofrequency ablation for single hepatocellular carcinoma. Hepatology 2001; 33:1124–1129.
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32. Rhim H, Dodd GD 3rd. Radiofrequency thermal ablation of liver tumors. J Clin Ultrasound 1999; 27:221–229. 33. Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Solbiati L, Gazelle GS. Small hepatocellular carcinoma: treatment with radiofrequency ablation versus ethanol injection. Radiology 1999; 210: 655–661.
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34. Rossi S, Di Stasi M, Buscarini E, et al. Percutaneous RF interstitial thermal ablation in the treatment of hepatic cancer. AJR Am J Roentgenol 1996; 167:759–768. 35. Kaplan U, Hatoum OA, Chulsky A, Menzal H, Kopelman D. Two weeks delayed bleeding in blunt liver injury: case report and review of the literature. World J Emerg Surg 2011; 6:14.
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Figure E1. A 50-year-old man presented with progressively decreased levels of hemoglobin after RF ablation for hepatocellular carcinoma. (a) CT scan obtained 2 hours after RF ablation shows a pseudoaneurysm (arrow) at an anterior aspect of the ablation site (asterisk) with anterior abdominal hematoma and hemorrhagic ascites along the course of the needle tract. (b, c) Coronal reformatted CT image shows a pseudoaneurysm (arrow) (b) from the branch of the right internal thoracic artery, which was also shown on a right internal thoracic angiogram (arrow) (c). (d) On nonenhanced CT image obtained after embolization, abdominal hematoma and hemorrhagic ascites were nearly resolved after embolization with a combination of gelatin sponge particles and 1 microcoil (arrow) for the right internal thoracic artery.
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Figure E2. A 53-year-old man presented with hemoperitoneum after RF ablation. (a) Enhanced CT image shows a small hepatocellular carcinoma (arrow) in segment VII adjacent to the diaphragm. (b) CT image obtained immediately after ablation shows contrast medium extravasation near the bare area, resulting in hemoperitoneum (arrow). (c) Right inferior phrenic angiogram reveals contrast medium extravasation (arrowheads) from the branches of the right inferior phrenic artery. (d) Right inferior phrenic angiogram after embolization using N-butyl cyanoacrylate demonstrates no further extravasation of the contrast medium.