Abstract
Objective:
To evaluate the hemostatic efficacy of re-radiofrequency ablation (re-RFA) for hepatic tract bleeding after ultrasound-guided RFA of hepatic tumors.
Methods:
A total of 4679 percutaneous ultrasound-guided RFA procedures were performed for hepatic tumors at Samsung Medical Center between January 2012 and December 2020. We identified patients who had hepatic tract bleeding after RFA by reviewing radiologic reports and ultrasound images and investigated the measures taken to control the bleeding and their outcomes. We also identified patients who had a significant peritoneal hematoma on immediate post-RFA CT or underwent transarterial embolization to control hepatic bleeding after RFA of hepatic tumors.
Results:
In total, 91 patients with tract bleeding after RFA were identified. As initial measures to control the bleeding, external compression, re-RFA, and observation were performed in 71 (78%), 17 (19%), and 3 (3%) patients, respectively. Hemostasis using re-RFA was attempted to control tract bleeding in 40 patients as an initial measure or an additional measure after other initial efforts. In all 40 patients, the bleeding stopped after re-RFA on Doppler ultrasound, and there was no active bleeding on the immediate follow-up CT. During the study period, in the years when re-RFA was performed frequently, the number of transarterial embolizations to control tract bleeding and significant peritoneal hematoma formation tended to be low.
Conclusion:
Hemostasis using re-RFA of the needle tract is effective in controlling tract bleeding after ultrasound-guided RFA of hepatic tumors.
Advances in knowledge:
Re-RFA is a simple, safe, and effective method to control tract bleeding.
Introduction
Radiofrequency ablation (RFA) is a widely used treatment for small hepatocellular carcinoma (HCC) or liver metastasis.1–4 Although RFA is minimally invasive and relatively safe, various complications can occur. The major complication rates after percutaneous RFA for hepatic tumors have been reported to range from 1.9 to 5.2%.5–10 The reported major complications include abscess, tumor seeding, hemorrhage, ground pad burn, pneumothorax, hemothorax, biliary tract injury, diaphragmatic injury, and bowel perforation.6,9
Intra-abdominal hemorrhage is a common complication of RFA for hepatic tumors. Rhim et al6 reported that the incidence of peritoneal hemorrhage was 0.46%, and Akahane et al9 reported that the incidence of hemorrhage requiring transfusion was 0.4%. Intra-abdominal hemorrhage is usually thought to result from direct injury of the blood vessels by the RF electrodes. Venous bleeding stops spontaneously or can be controlled by conservative management, such as external compression of the liver. On the other hand, arterial bleeding is more severe and may require endovascular intervention or surgery. Cauterization of the needle tract is recommended to decrease the risk of hemorrhage when pulling out the electrode after tumor ablation.11 If bleeding persists despite conservative treatment, it can be life threatening. In this case, transarterial embolization is considered the treatment of choice to control the bleeding.12 However, if different physicians and procedure rooms are involved in performing the RFA and transarterial embolization, transarterial embolization can be delayed. In fact, according to a previous study, the median time interval between symptom presentation and angiography was as long as 22 h.12
In our institution, as one of the methods to control tract bleeding, re-RFA, the method of ablating the bleeding focus after reinserting the electrode, has been used. In this study, we evaluated the hemostatic efficacy of re-RFA for hepatic tract bleeding after percutaneous ultrasound-guided RFA of hepatic tumors.
Methods and materials
This retrospective study was conducted at an academic tertiary referral center. The study protocol conformed to the ethical guidelines of the 1975 Declaration of Helsinki, and the Institutional Review Board of our institution approved this study and waived the need for written informed consent.
Patients
A total of 4679 percutaneous ultrasound-guided RFA (4033 patients with HCCs and 646 patients with hepatic metastases) were performed at Samsung Medical Center between January 2012 and December 2020.
Percutaneous ultrasound-guided RFA procedure
RFA was performed by one of the five radiologists with more than 3 years of experience in locoregional treatments for hepatic tumors. RFA was performed percutaneously under US guidance (LOGIQ E9 or E10, GE Healthcare, Milwaukee, WI). We used commercially available generators (VIVA Multi RF generator, STARmed, Goyang, Korea or M-3004 System, RF Medical, Seoul, Korea) with a 15- or 17-gauge single internally cooled electrode (Proteus, STARmed), a 17-gauge single internally cooled wet electrode (Jet-Tip, RF Medical, Seoul, Korea), or 15- or 17-gauge multiple internally cooled electrodes (Octopus, STARmed) depending on the tumor size and location. The number of puncture of the liver capsule with an electrode to access the lesion was as follows: mean, 2.3; median, 2; range, 1–6. Procedures were performed under conscious sedation or monitored anesthesia care, while the latter was controlled by trained anesthesiologists. After complete ablation of the hepatic tumors, we routinely cauterized the needle tract by slowly pulling out the electrode while maintaining the temperature around the electrode tip at approximately 60–80°C. After tract cauterization, Doppler ultrasound was performed to check for tract bleeding. Contrast-enhanced liver CT was performed within 12 h of RFA to evaluate the therapeutic outcomes and possible complications.
Re-RFA for tract bleeding
Re-RFA was performed after the RF electrode was reinserted into the bleeding focus under ultrasound guidance (Figure 1). Unlike tract cauterization, which is routinely performed when the electrode is removed after tumor ablation, re-RFA for hemostasis was served with a power of 100 W or more to overcome the heat-sink effect caused by bleeding. In addition, the cooling pump was not stopped when attempting bleeding control to ensure that the ablation zone covered the bleeding focus. If the active tip of the electrode could be adjusted, the length of the active tip was adjusted to 1.0–1.5 cm to minimize adjacent hepatic parenchymal injury. Ablation time was usually less than 5 min.
Figure 1.
A 54-year-old male patient underwent immediate hemostasis using re-RFA for hepatic tract bleeding after percutaneous ultrasound-guided RFA of HCC. (a) There was a 1.9 cm HCC in segment VI of the liver (white arrow). Massive ascites was seen at perihepatic space (asterisks). (b) Percutaneous ultrasound-guided RFA was performed using a 15-gauge adjustable electrode with a 2.5 cm active tip. (c) After ablation of the tumor and withdrawal of the electrode, hepatic bleeding through the electrode tract was detected on color Doppler ultrasound (white arrowheads). (d) The hepatic bleeding showed pulsatile waveform on spectral Doppler ultrasound. (e) The active tip of the same electrode used for tumor ablation was adjusted to 1.5 cm, and the electrode was reinserted into the bleeding focus. Ablation was conducted using a power of 100–200 W for about three minutes. A cooling pump was not stopped during ablation to create a sufficient ablation zone, covering the bleeding tract. (f) No more hepatic tract bleeding was seen on follow-up color Doppler ultrasound immediately after ablation of bleeding focus. (g) On the immediate follow-up CT, the index tumor was ablated completely (black arrow). There was a large amount of ascites at the perihepatic space, but there was no extravasation of contrast media or hematoma formation. (h) Another small ablation zone created as a result of re-RFA for hemostasis was seen below the index tumor (black arrowhead). HCC, hepatocellular
Data acquisition
We reviewed radiologic reports and ultrasound images to identify patients who had hepatic tract bleeding after percutaneous ultrasound-guided RFA for hepatic tumors. In patients with tract bleeding after RFA, we investigated the measures taken to control tract bleeding and the outcomes of these measures. In addition, the presence of active hepatic bleeding and the amount of bleeding were determined on immediate post-RFA CT. The baseline characteristics of these patients and their tumors were obtained by reviewing the electronic medical records of our institution.
In all patients who underwent percutaneous US-guided RFA for hepatic tumors during the study period, we reviewed radiologic reports and CT images to identify patients who had a peritoneal hematoma on immediate post-RFA CT and investigated whether transfusion of red blood cells (RBCs), transarterial hepatic embolization, or surgery for hemostasis was performed. Hemoglobin levels before and within 3 days after RFA were recorded. A decrease in hemoglobin level of more than 1 g dl−1 was defined as a significant decrease in hemoglobin level.
To measure the amount of bleeding, a region of interest was placed at the margin of the hematoma on immediate post-RFA CT images. An acute hematoma usually appears to be a high-attenuation fluid (generally higher than 30 HU) in the perihepatic space or dependent portion of the peritoneal cavity. The amount of bleeding was calculated by the summation of all hematoma areas in each slice, multiplied by the slice thickness. A significant peritoneal hematoma was defined as a hematoma of ≥150 ml. Since there is no reference material to use as a criterion for the definition of a significant peritoneal hematoma, about half a unit of packed RBC was uses as a criterion.
Results
A total of 91 patients with tract bleeding after percutaneous ultrasound-guided RFA of hepatic tumors were identified. The demographics of the 91 patients are summarized in Table 1.
Table 1.
Demographics of patients who underwent re-RFA to control tract bleeding after RFA
| Age (yr) | 62.1 ± 9.5 (35–83) |
| Sex (M / F) | 69/22 |
| Tumor | |
| Diagnosis (HCC / metastasis) | 78/13 |
| Tumor size (cm) | 1.7 ± 0.7 (0.4–4.3) |
| Tumor number (1/2) | 80/11 |
| Hb (g/dl) | 12.2 ± 2.1 (6.1–17.0) |
| Platelet (x103/ul) | 113.2 ± 63.9 (45.0–438.0) |
| PT(INR) | 1.1 ± 0.2 (0.9–1.6) |
| Child-Pugh class (A / B / C) | 86/4/1 |
HCC, Hepatocellular carcinoma; Hb, Hemoglobin; PT (INR), Prothrombin time (international normalized ratio); RFA, Radiofrequency ablation.
Note. Data are means ± standard deviation with ranges in parentheses.
Initial management of tract bleeding
Figure 2 shows the measures taken to control the tract bleeding. External compression was used as an initial measure of bleeding control in 71 (78%) of the 91 patients. Immediate re-RFA was performed in 17 (19%) patients under the operator’s judgment that it would be difficult or time-consuming to control the tract bleeding by external compression. In three (3%) patients, an observation was performed without any other measures under the judgment of the operator that external compression would not be effective due to the large amount of ascites.
Figure 2.
Management of tract bleeding and outcomes.
The outcome of external compression for tract bleeding control
Tract bleeding was controlled after external compression for less than approximately 5 min in 38 (54%) of 71 patients, and continued despite approximately 5 min of external compression in 33 (46%) of 71 patients. Additional external compression was performed in 11 of 33 patients, and tract bleeding was controlled in 9 of them. The remaining two patients underwent re-RFA or transarterial embolization because the tract bleeding continued even with additional external compression. In all 11 patients, there was a significant decrease in hemoglobin level or significant peritoneal hematoma on the immediate post-RFA CT: a significant decrease in hemoglobin level and a significant peritoneal hematoma in six patients, a significant decrease in hemoglobin level without a significant peritoneal hematoma in three patients, and a significant peritoneal hematoma without a significant decrease in hemoglobin level in two patients. The three patients who had a significant decrease in hemoglobin level without a significant peritoneal hematoma had a moderate amount of ascites. Therefore, it is possible that ascites diluted the extravasated blood, and the amount of bleeding was underestimated.
The outcome of re-RFA for tract bleeding control
Hemostasis using re-RFA was attempted for hepatic tract bleeding in 40 patients: immediate re-RFA as an initial measure to control tract bleeding in 17 patients, re-RFA after approximately 5 min of observation in 1 patient, re-RFA after approximately 5 min of external compression in 21 patients, and re-RFA after 20 min of external compression in 1 patient. On immediate follow-up Doppler ultrasound after re-RFA for hemostasis, the bleeding stopped in all patients. There was no extravasation of contrast media, indicating active bleeding in any patient on the immediate follow-up CT.
In one patient who underwent re-RFA after approximately 20 min of external compression, there was a significant peritoneal hematoma on immediate post-RFA CT. One patient who underwent re-RFA after 5 min of external compression received RBCs transfusion because hemoglobin level decreased from 8.2 to 6.8 g dl−1 the day after the RFA. In one patient who underwent re-RFA after 5 min of observation, hemoglobin level decreased from 9.5 to 8.4 g dl−1 the day after the RFA. Except for these three patients, there was no significant peritoneal hematoma on the immediate follow-up CT or a significant decrease in hemoglobin level.
In all patients, no complications related to re-RFA were observed.
Annual number of significant peritoneal hematoma formation and transarterial embolization
Figure 3 shows the annual number of significant peritoneal hematoma formation on immediate post-RFA CT, transarterial embolization to control hepatic bleeding, and re-RFA to control tract bleeding. In 2016, 2018, 2019, and 2020, when re-RFA was performed frequently, transarterial embolization to control hepatic bleeding was never performed. The frequency of significant peritoneal hematoma formation tended to be lower than that in the other years.
Figure 3.
The annual number of transarterial embolization, significant peritoneal hematoma formation on immediate follow-up CT, and hemostasis using re-RFA during the study period.
Discussion
In our study, we introduced a hemostatic method using re-RFA to control hepatic tract bleeding after ultrasound-guided RFA of hepatic tumors and showed that this method was effective. During the study period, hemostasis using re-RFA to control tract bleeding after RFA of hepatic tumors was performed in 40 patients. The tract bleeding stopped on immediate follow-up Doppler ultrasound, and active bleeding was not observed in any of the patients on immediate follow-up CT. Although our immediate hemostasis strategy was beneficial, in some patients, the bleeding may have stopped spontaneously without using this method. However, in the years when re-RFA was frequently performed, the number of transarterial embolizations to control hepatic bleeding and the number of significant peritoneal hematoma formations tended to be low. These results indirectly indicate that this method can be effective against acute tract bleeding that does not stop on its own and may require additional treatment. Given that tract bleeding after percutaneous RFA can be life threatening if neglected or improperly managed, our immediate hemostasis method using re-RFA would be a simple and effective strategy for patient management. Moreover, it does not require additional medical resources, patients and doctors’ anxiety, and cost. Therefore, if hepatic bleeding is detected on Doppler ultrasound after RFA of hepatic tumors, it is recommended to try immediate hemostasis with this method first, and if this method does not work, to try embolization or surgery.
There are a few case reports related to the use of RFA for hemostasis of hepatic bleeding.13–15 In these case reports, RFA was used to control massive hemorrhage from ruptured hepatic tumors or blunt liver trauma. In all reported cases, RFA was performed under laparotomy, not percutaneously, but hemostasis using RFA was successful despite massive bleeding. Compared to these challenging hemostasis with RFA, re-RFA of tract bleeding after percutaneous RFA would be a simple and effective method as the bleeding focus can be easily identified along the needle track on color Doppler US. This assumption is highly supported by the high success rate (100%, 40/40) of re-RFA for tract bleeding in the present study. Furthermore, using the immediate hemostasis strategy, we do not have to risk the patient’s hemodynamic instability due to delayed management.
Although the effect of tract cauterization after percutaneous RFA has been controversial,16 tract cauterization has been routinely performed after RFA of hepatic tumors to avoid tract bleeding and tract seeding. However, bleeding in the hepatic tract continues to occur. These results suggest that tract cauterization has only a limited effect in preventing major hepatic bleeding. This is possible because tract cauterization is performed while the electrode is pulled out; therefore, sufficient energy to stop bleeding is not delivered. In our study, re-RFA for immediate hemostasis was performed with high energy, focusing on the bleeding area. We also created a small ablation zone covering the bleeding focus; therefore, immediate hemostasis was thought to be successful.
In 38 of 71 patients, tract bleeding stopped with approximately 5 min of compression. Therefore, immediate re-RFA in all patients with tract bleeding is likely to be overtreated, which can be considered in the following cases. First, re-RFA can be useful if tract bleeding persists even after 5 min of compression. In 9 of 11 patients who underwent additional compression after 5 min of compression due to persistent bleeding, the tract bleeding stopped, but there was a significant decrease in hemoglobin or significant peritoneal hematoma in all patients. In addition, 2 of the 11 patients had to undergo either re-RFA or transarterial embolization because the tract bleeding persisted despite additional compression. In contrast, in most patients (20 of 21 patients) who underwent re-RFA after approximately 5 min of compression, there was no significant decrease in hemoglobin level and a significant peritoneal hematoma. Therefore, we believe that re-RFA is useful if tract bleeding persists even after 5 min of compression. Second, re-RFA can be considered as an initial measure to control tract bleeding in patients with large amounts of ascites because external compression may not be effective in controlling tract bleeding. Third, re-RFA can be considered an initial measure if the pulsatile waveform is identified on Doppler ultrasound or if the bleeding rate is determined to be fast.
This study has the inherent limitations of a retrospective study. First, patients with tract bleeding were identified by reviewing radiologic reports and ultrasound images. Some operators may not have reported tract bleeding that had been stopped by manual compression or observation. Therefore, the proportion of patients whose bleeding was controlled only by compression may have been underestimated. Second, the method of controlling tract bleeding varied depending on the operator and the year of treatment. In fact, before 2016, only one radiologist intermittently used re-RFA for hemostasis in our institution. After sharing this method with all radiologists in 2016, an agreement was reached to use it, and all radiologists started trying it out. Therefore, to verify our initial experience, a well-designed prospective multicenter study is warranted.
In conclusion, hemostasis using RFA is effective for treating tract bleeding after percutaneous ultrasound-guided RFA of hepatic tumors. Considering the simplicity and safety of re-RFA, we recommend using this method in patients whose tract bleeding persists despite compression or whose tract bleeding is not expected to stop with compression.
Contributor Information
Kyoung Doo Song, Email: kd3893.song@samsung.com.
Min Woo Lee, Email: leeminwoo0@gmail.com.
Hyunchul Rhim, Email: hc.rhim@samsung.com.
Tae Wook Kang, Email: kaienes.kang@samsung.com.
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