Abstract
Purpose: The aim of the study was to prospectively evaluate the safety and effectiveness of percutaneous microwave (MW) ablation for liver cancer adjacent to the diaphragm.
Materials and methods: From May 2005 to June 2008, 89 patients with 96 hepatic lesions adjacent to the diaphragm (the shortest distance from the lesion margin to the diaphragm less than 5 mm), who underwent ultrasound (US)-guided percutaneous MW ablation, were included in the study group. A total of 100 patients with 127 hepatic lesions not adjacent to the diaphragm (the shortest distance from the lesion to the diaphragm and the first or second branch of the hepatic vessels more than 10 mm), who underwent US-guided percutaneous MW ablation, were included in the control group. During the ablation the temperature of marginal ablation tissue proximal to the diaphragm was monitored and controlled at 50°–60°C for more than 10 min in the study group. We compared the results of ablation between the two groups.
Results: A total of 91 of 96 tumours (94.8%) in the study group and 123 of 127 tumours (96.9%) in the control group achieved complete ablation (P > 0.05). Local tumour progression was found in 18 of 96 tumours (18.8%) in the study group and 21 of 127 tumours (16.5%) in the control group during follow-up after MW ablation (P > 0.05). No major complications occurred in either group.
Conclusions: Under strict temperature monitoring, percutaneous MW ablation is safe and can achieve a high complete ablation rate for the treatment of hepatic tumours adjacent to the diaphragm.
Introduction
Hepatocellular carcinoma (HCC) is one of the most common malignant tumours in the world Citation[1], Citation[2]. The liver is also the most common organ involved in metastatic disease Citation[3]. For the past few years, non-surgical treatment modalities have been developed in treating primary and metastatic hepatic tumours Citation[4], Citation[5]. Image-guided thermal ablation using different energy sources (such as radiofrequency, microwave, or laser) has been proven to play a valuable role against hepatic tumour Citation[6–13]. The benefits of thermal ablation include low morbidity, few complications and repeatability for recurrence Citation[12–21].
A pervasive idea among doctors is that percutaneous thermal ablation of hepatic tumours adjacent to the diaphragm poses a substantial risk of diaphragmatic injury Citation[10], Citation[11], Citation[15], Citation[21]. Some authors have recommended that percutaneous thermal ablation should be avoided when treating liver tumours adjacent to the diaphragm, or that special interventional techniques are necessary to separate the diaphragm from the liver, and have achieved a high complete ablation rate Citation[22], Citation[23]. Our previous in vivo experimental study showed that microwave (MW) ablation for liver tissue adjacent to the diaphragm is safe by monitoring the temperature of the ablation area fluctuating between 50°–60°C Citation[24]. Thermal injury may be prevented by strict temperature monitoring of hepatic tissue adjacent to important organs or structures. The purpose of this prospective study was to assess the safety and effectiveness of percutaneous MW ablation for liver tumours adjacent to the diaphragm.
Materials and methods
Study population
From May 2005 to June 2008, 1382 patients with HCC or metastatic liver cancer underwent percutaneous MW ablation with curative intention at our institution. Indication criteria for MW ablation were unresectable tumour or patient's refusal to undergo surgery; tumour accessible via a percutaneous approach; single nodular HCC lesions of 6.0 cm or smaller; three or fewer multiple nodular hepatic lesions with a maximum diameter of 4.0 cm or less in each nodule; absence of portal vein thrombosis or extrahepatic metastases; prothrombin time of less than 25 s, prothrombin activity higher than 40%, and platelet count higher than 40 cells × 109/L.
Of 1382 patients who underwent MW ablation, 1193 patients were excluded from the study for the following reasons: new lesions were found after our previous MW ablation; new lesions were found after transcatheter arterial chemoembolisation (TACE), radiofrequency (RF) ablation, or other therapy; patients underwent immunotherapy accompanied by our MW ablation; patients were lost to follow-up. Thus, 189 patients with 223 hepatic lesions were included in our study. A total of 89 patients with 96 hepatic lesions adjacent to the diaphragm (the shortest distance from the lesion margin to the diaphragm less than 5 mm) who underwent ultrasound (US)-guided percutaneous MW ablation were included in the study group. A total of 100 patients with 127 hepatic lesions not adjacent to the diaphragm (the shortest distance from the lesion margin to the diaphragm and the first or second branch of the hepatic vessels more than 10 mm), who underwent US-guided percutaneous MW ablation, were included in the control group. The shortest distance from the lesion margin to the diaphragm was confirmed by contrast enhanced computerised tomography (CT) or magnetic resonance imaging (MRI) in transverse plane and coronal plane. In total, 56 men and 33 women were included in the study group, with a mean age of 60.1 ± 9.72 years (age range, 36–74 years). In total, 66 men and 34 women were included in the control group, with a mean age of 58.34 ± 11.6 years (age range, 29–81 years). In total, 64 patients with 67 lesions had HCC and 25 patients with 29 lesions had liver metastatic disease in the study group. In the control group 76 patients with 95 lesions had HCC and 24 patients with 32 lesions had liver metastatic disease. Among the 61 liver metastatic lesions, 18 were from colorectal cancer, 13 from gynaecologic cancer, 10 from breast cancer, 9 from gastric cancer, 8 from lung cancer, 2 from prostate cancer, and 1 from oesophageal cancer. The pre-ablation Child–Pugh classification was performed in all patients: 72 patients (80.9%) in the study group and 89 patients (89%) in the control group had class A disease, and 17 patients (19.1%) in the study group and 11 patients (11%) in the control group had class B disease. The median follow-up periods of the study group and the control group were 15 and 17.5 months.
This investigation was approved by our institutional Ethics Committee. Written informed consent was obtained from all patients.
There was no significant difference in clinical backgrounds between the study group and control group ().
Table I. Comparison of clinical data in the study and control groups.
Pre-ablation imaging work-up and histological diagnosis
Pre-treatment examination included sonography, contrast-enhanced sonography, contrast-enhanced CT and/or contrast-enhanced MR, and tumour marker assay in all subjects. The maximum diameters of the tumours were measured on contrast-enhanced sonography. Ultrasound and contrast-enhanced sonography were performed using an ACUSON Sequoia 512 (Mountain View, CA, USA) with a 3.5∼5.0 MHz 4V1 transducer. Ultrasound contrast agent was SonoVue (Bracco, Milan, Italy).
Histological diagnosis was obtained by ultrasound-guided tumour biopsy using an 18-gauge needle in all patients. In patients with multiple nodules, at least one biopsy was performed. If new tumours emerged after ablation, biopsies for the new nodules were performed.
Laboratory data
Since an increase in serum alpha-fetoprotein (AFP) levels may indicate recurrence or new lesions, AFP assay was performed in all patients before and after MW ablation. The AFP level was abnormal (range, 23∼7800 µg/L) in 53 patients in the study group and 61 patients in the control group. The AFP level was normal (≤20 µg/L) in the remaining 75 patients. Serum AFP assay was performed 1 month after MW ablation, and follow-up was performed at an interval of 3 months.
Microwave ablation procedure
All treatments were performed in our institution and were carried out under US guidance with the patients under unconscious intravenous anaesthesia (propofol, 6–12 mg/kg/h; ketamine, 1–2 mg/kg) in the operating room. The microwave unit (KY-2000, Kangyou Medical, Nanjing, China) consists of three independent microwave generators, three flexible coaxial cables and three water pumping machines, which can drive three cool-tip needle antennas. The generator is capable of producing 1∼100 W of power at 2450 MHz. The antenna was 15 gauge in diameter with cool-shaft. Under US guidance, a single antenna or multiple antennae were used, depending on the tumour size. All therapy was performed by two experienced radiologists, each having more than 10 years of experience with interventional procedures. A detailed protocol, which included the placement of the antennae, power output setting, microwave emission time, and appropriate approach, was worked out for each patient on an individual basis before treatment. All patients were placed in a supine or left-lateral position depending on the operation plan and tumour location. To completely visualise the tumours located in posterior segment VII or segment VIII, some patients were asked to take a deep breath and hold their breath for a few seconds. After the tumours were visualised and the puncture points were decided by US, the skin marks were made, and the puncture sites were routinely disinfected. Then, the antennae were inserted through the intercostal spaces and directed upwards to approach the tumours immediately under the diaphragm. For tumours at the dome, which were too difficult to visualise by US and to approach, we used artificial pleural effusion to increase tumours’ conspicuity and to avoid transthoracic routes. An 18-gauge needle was inserted into the pleural cavity under US guidance and 345–820 mL (mean ± SD, 510 ± 110 mL) normal saline (0.9%) was rapidly injected to produce the artificial pleural effusion until the tumour and the needle tract were visualised clearly. Microwave generators were started when the ends of the antennae were located in the expected positions of the lesions. In general, for tumours less than 2.0 cm in diameter, a single antenna was used; multiple antennae were required for tumours 2.0 cm or larger. A power output setting between 40 W and 60 W was used during ablation with continuous or intermittent emission. During the therapy, we monitored the hyperechoic area of ablation using grey-scale sonography and thermal monitoring to decide the endpoint of treatment. After ablation of the tumours, the antennae were slowly withdrawn, and MW emission was continued until the antennae were pulled to just under the skin entrance site. This method allowed needle track cauterisation to prevent tumour seeding and to minimise bleeding after ablation. The MW ablation was performed under real-time US guidance (ACUSON Sequoia 512) by one experienced radiologist. Within 3 days of ablation every patient received contrast-enhanced sonography to evaluate the ablation area. If residual tumour or unablated therapeutic margin was detected, additional MW ablation treatment was performed.
Thermal monitoring procedure
A thermal monitoring system attached to the microwave unit was used during treatment for the study group. With US guidance, one or two 21-gauge thermal monitoring needles (Kangyou Medical) were placed into marginal tissue of tumour or liver proximal to the diaphragm for real-time temperature monitoring during the ablation to protect the diaphragm from thermally mediated injury. Based on our experimental evidence and clinical experience, the temperature cut- off point for ablation therapy was set at 60°C in the patients. If the measured temperature reached 60°C, emission of microwave antenna was stopped immediately and was restarted after the temperature decrease to 50°C. The measured temperature was controlled to between 50°C and 60°C for more than 10 min ().
Figure 1. The curve of temperature monitoring during MWA for tumour adjacent to diaphragm. The temperature of marginal tissue of tumour adjacent to diaphragm was monitored and controlled to fluctuating between 50°C and 60°C for 610 s during the whole treatment procedure.
Follow-up imaging
The follow-up protocol was performed according to previously published recommendations Citation[12], Citation[23]. The follow-up period was calculated starting from the beginning of MW ablation in all patients. Therapeutic effectiveness was assessed on the basis of an integrative evaluation of contrast-enhanced imaging and serum tumour marker levels. Contrast-enhanced CT or MRI and contrast-enhanced sonography were repeated at 1-month and then at 3-month intervals in the first year after microwave ablation treatment and then at 6-month intervals.
Assessment of safety
For the assessment of safety, we evaluated whether any complications occurred during the therapy procedure and follow-up period. The description of complications in this study follows the proposed standardisation of terminology and reporting criteria Citation[12]. Major complications are described as conditions that may lead to death if untreated, as well as conditions resulting in substantial morbidity and disability. All other complications were considered to be minor complications.
Statistical analysis
Statistical analysis was performed using SPSS for windows (Version 10.0) and the data expressed as means ± standard deviation (SD). Independent samples t-test was used to compare the means between the groups and chi-square test was undertaken to compare the proportions. P < 0.05 was considered to indicate a significant difference.
Results
Outcome of microwave ablation
All patients were successfully treated. No more than 3 sessions were performed to complete the treatment (1 session for 63, 2 sessions for 30, 3 sessions for 3, mean 1.3 ± 0.4 sessions per patient) in the study group. Out of 96 tumours in the study group and 127 tumours in the control group, 91 (94.8%) and 123 (96.9%), respectively, achieved complete ablation as confirmed at 1 month after MW ablation by contrast CT or MRI (). No significant statistical difference in the rate of complete ablation was found between the study group and the control group (P > 0.05). In all 223 tumours of the study, 158 of 162 (97.5%) HCCs and 56 of 61 (93.3%) metastatic hepatic tumours achieved complete ablation, and significant statistical difference was found between HCC and metastatic hepatic tumours (P < 0.01). Total treatment duration for one nodule was 660∼1840 s in the study group and 180∼1620 s in the control group. Although the size of tumours in the study group had no significant difference with that in the control group, nodules in the study group required longer duration of ablation than those in the control group; however, they did not require a larger number of treatment sessions ().
Figure 2. Liver cancer abutting dome of the diaphragm of a 65-year-old man treated with MWA. (A) Before ablation, tumour (arrowhead) is seen in MRI scans. (B) One day after ablation, the ablated zone (arrowhead) was evaluated by contrast enhanced sonography. (C) One month after ablation, the ablation zone (arrowhead) has no arterial enhancing in MRI scans. (D) Six months after ablation, MRI coronal plane scans show the diaphragm (arrowhead) has not been destroyed and the ablation zone has no local tumour progression.
Table II. Comparison of therapeutic data in the study and control groups.
Tumour marker (AFP) changes
The AFP level was abnormal (>20 µg/L) in 53 patients in the study group and 61 patients in the control group. Among the 53 patients in the study group, 25 of 53 (47.2%) patients’ AFP levels showed a completely negative result in AFP assay, and 18 of 53 (34%) showed the AFP level decreasing by more than 50% 1 month after the ablation. Among the 61 patients in the control group, 33 of 61 (54.1%) showed a completely negative result in AFP, and 17 of 61 (27.9%) showed AFP level decreasing by more than 50% 1 month after the ablation. There was no significant statistical difference in the rate of AFP level decrease between the study group and the control group (P > 0.05).
Complications and side effects
There were neither immediate nor periprocedural major complications in both study and control groups. In the study group, on a scale of mild, moderate or severe, 9 cases (10.1%) suffered mild or moderate right shoulder pain which ranged in duration from 2 to 13 days, with a mean duration of 6.5 days; 2 cases (2.2%) suffered severe right shoulder pain which needed analgesics to control, and ranged in duration of 10 days, followed by mild pain for 2 months, and 21 cases (23.6%) developed pleural effusion. Of these 21 cases 18 cases had a small amount of pleural effusion and had the symptoms self-relieved in 1 week, and 3 cases had a moderate or great amount of pleural effusion and were treated by placement of a tube drain. Nausea and vomiting developed in 8 cases (9.0%) and disappeared within 1 to 2 days after ablation. In the control group, only 1 (1.0%) case suffered mild right shoulder pain for 2 days; 4 cases (4.0%) developed a small amount of pleural effusion that ranged in duration from 2 to 7 days; 1 case developed nausea and vomiting after ablation. The study group had significantly higher rates of symptoms such as the shoulder pain, pleural effusion and nausea and vomiting than those in the control group ().
Table III. Complications following percutaneous microwave ablation between the study group and control groups.
Local tumour progression
Local tumour progression was found in 18 of 96 tumours (18.8%) in the study group and in 21 of 127 tumours (16.5%) in the control group by follow-up contrast-enhanced imaging. No significant statistical difference in the local tumour progression rate was found between the study group and the control group (P > 0.05). The maximum diameter of tumours and the number of sessions were not significant predictors of local tumour progression (P > 0.05) (). Out of 162 HCCs and 61 metastatic hepatic tumours, 20 (12.3%) and 19 (31.1%), respectively, had local tumour progression, and a significant statistical difference was found between HCCs and metastatic hepatic tumours (P < 0.01).
Table IV. Comparison of maximum diameter sessions and type of tumours in the completely ablated lesions and local tumour progression lesions.
Discussion
Sonography-guided percutaneous thermal ablation is a widely accepted method for treatment of malignant liver tumours Citation[25], Citation[26]. Although thermal ablation is considered safe, several complications are associated with all thermal therapies Citation[27], Citation[28]. The major concern for thermal ablation for tumours adjacent to the diaphragm rather than for tumours in other sites is diaphragm perforation. Percutaneous ablation for tumours adjacent to the diaphragm has not been well accepted in the past due to tumour location and RF ablation systems. Tumours located adjacent to the diaphragm always have a limited sonic window due to overlapped lung or ribs, and the tumours are difficult to approach. RF ablation systems show some unfavourable factors for percutaneous ablation. First, most thermal RF ablation systems incorporate multi-tined expandable electrodes, which are not able to confirm the positions of the retractable curved electrodes using sonography, and the electrodes may have to be placed in the diaphragm and may directly heat it. Second, not all RF ablation electrodes are internally cooled, and the temperature of ablation area can be hard to monitor. In addition, repeated ablations are blind due to outgassing during the therapy. Thus diaphragm injury and incomplete ablation of the tumours may result. Some authors have reported fatalities involving diaphragmatic complications of percutaneous RF ablation Citation[29], Citation[30]. Additionally, an animal study Citation[31] showed that RF ablation frequently leads to liver surface injury and adjacent trans-diaphragmatic injury near ablation sites. Although diaphragm injuries are rarely life threatening, they can be quite distressing to patients. Therefore, any method that can decrease the risk of diaphragm injury during ablation would help decrease complications and increase the number of patients who are eligible to undergo the procedure.
Microwaves could offer more direct heating than other energies, making MW ablation more potent in organs with high blood perfusion or near vascular heat sinks as compared with other thermo-ablative modalities, and the MW ablation zones are uniform in shape and size and remain unaffected by convective heat loss Citation[32], Citation[33]. These advantages have made MW ablation a widely used for treatment of hepatic tumours over recent years Citation[4], Citation[5], Citation[8], Citation[19], Citation[20].
Our results provide evidence that under strict temperature monitoring, MW ablation for tumours adjacent to the diaphragm can be performed safely. Of 89 patients with 96 tumours adjacent to the diaphragm, only 11 cases (12.3%) developed right shoulder pain after ablation, which was mild or moderate and rapidly self-relieved in 9 cases and severe in 2. The severe pain in the two cases disappeared within 2 months. These cases developed right shoulder pain and 21 cases developed pleural effusion, and we consider these complications could be associated with the heating irritation of the diaphragm Citation[27], Citation[34]. Some authors have reported this complication evidenced by focal, nodular diaphragmatic thickening adjacent to the ablation site on follow-up CT Citation[35], Citation[36]. In our study group, the diaphragm had not obviously changed on follow-up imaging after ablation.
In our study, four tumours in four cases were at the diaphragmatic dome and too difficult to visualise with US and to approach percutaneously. We used artificial pleural effusion to increase nodule conspicuity. Normal saline (0.9%) is an isosmotic solution (308 mosmol/L) that is well tolerated in virtually every body cavity. In this study, saline also appeared to have a protective effect, probably because of thermal buffering. The four tumours were treated successfully and patients did not develop right shoulder pain or upper quadrant pain. All of them achieved complete ablation and had no local tumour progression in the follow-up time ().
Figure 3. Hepatocellular carcinoma of a 45-year-old man. (A) The lesion (arrowhead) near the diaphragmatic dome and too difficult to be seen with US (left). After 1500 mL artificial pleural effusion, the lesion (arrowhead) was seen clearly (right). (B) One month after ablation, MRI scans show the lesion (arrowhead) was completely ablated in transverse plane (left) and coronal plane (right).
Although the size of tumours in the study group had no significant difference from that in the control group, nodules in the study group required longer duration of ablation than those in the control group because of intermittent emission of microwave antennae to avoid thermal damage to the diaphragm. However, the number of treatment sessions was not increased in our research, which benefited from detailed treatment protocol and accurate placement of antennae and tissue thermal monitoring needle. Based on our prior study of adult dogs, when the temperature of the liver margin adjacent to the diaphragm fluctuated between 50°C and 60°C lasting for more than 10 min, the diaphragm was not obviously damaged, as demonstrated by gross anatomy and histopathological examination immediately after ablation and at follow-up after ablation. We intended to control the temperature of marginal tissue of tumour or liver proximal to the diaphragm to lower than 60°C, the threshold temperature of coagulation, to obtain two goals: firstly to avoid thermal damage to the adjacent diaphragm, and secondly to ensure the thermal field covered the marginal tumour field. During the procedure, we especially observed the site of thermal monitoring needle by real-time ultrasound to prevent it from moving during patients’ respiration.
Our results of technical success may also be attributable to the fact that all MW ablation sessions were performed by two experienced radiologists, who began to perform US-guided percutaneous MW ablation for liver cancer in 1994. In addition, the ablation electrode used in the study was an internally cooled straight-needle electrode, and the advantage of the straight-needle electrode is greater visibility of the emission tip compared with the expandable electrode of RFA, which could protect the diaphragm from puncturing. Equally important, the straight-needle is easily drawn back during the ablation if the patient felt pain resulting from the diaphragm. These rational factors can decrease the risk of major complications. In our study, we found no significant difference between the study group and control group either in major complications or in the local tumour progression rate. Although there were no controlled studies of MW ablation versus other methods of treatment for tumours adjacent to the diaphragm, our results of technical safety and therapeutic effectiveness were close to the results in other studies Citation[35], Citation[36].
In our study, we achieved a higher complete ablation rate and lower local tumour progression rate in HCCs than in metastatic hepatic tumours. These outcomes may have resulted from the pathologic features of the tumours. Compared with metastatic hepatic tumour, HCC is more prone to forming a pseudocapsule, consisting mainly of peritumoural hepatic sinusoids and/or fibrosis Citation[37]. The pseudocapsule is an important pathologic feature of HCC, which may prevent free invasion of HCC to the host liver and also indicates a relatively positive prognosis after tumour therapy Citation[38]. With regard to tumours for thermal ablation, a pseudocapsule could make the heat from microwave antenna congregated in the tumours and thus achieve a higher complete ablation rate compared with metastatic tumours.
This study also had some limitations. First, we evaluated the thermal injury of the diaphragm only according to symptomatology and imaging appearances, not based on pathological proof. Second, these data were obtained from a single centre, and the follow-up time was short. A multicentre study with a larger number of patients and a prolonged observation time is required to observe further curative effect. Third, at present a thermal monitor can get only one temperature at one point. The research of temperature monitoring for multiple points with one thermal monitoring needle may be an objective for the evaluation of ablation effects in the future.
Conclusion
In conclusion, under strict temperature monitoring, percutaneous MW ablation is safe and can achieve a high complete ablation rate for the treatment of hepatic tumours adjacent to the diaphragm. This modality may provide a new way for the treatment of liver cancer adjacent to the diaphragm.
Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References
- Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74–108
- Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet 2003; 362: 1907–1917
- Bruix J, Fuster J, Llovet JM. Liver transplantation for hepatocellular carcinoma: Foucault pendulum versus evidence-based decision. Liver Transpl 2003; 9: 700–702
- Shiina S, Teratani T, Obi S, Hamamura K, Koike Y, Omata M. Nonsurgical treatment of hepatocellular carcinoma: From percutaneous ethanol injection therapy and percutaneous microwave coagulation therapy to radiofrequency ablation. Oncology 2002; 62: S64–68
- Haemmerich D, Laeseke PF. Thermal tumour ablation: Devices, clinical applications and future directions. Int J Hyperthermia 2005; 21: 755–760
- Seki T, Wakabayashi M, Nakagawa T, Itho T, Shiro T, Kunieda K, et al. Ultrasonically guided percutaneous microwave coagulation therapy for small hepatocellular carcinoma. Cancer 1994; 74: 817–825
- Ryan TP, Turner PF, Hamilton B. Interstitial microwave transition from hyperthermia to ablation: Historical perspectives and current trends in thermal therapy. Int J Hyperthermia 2010; 26: 415–433
- Dong BW, Liang P, Yu XL, Zeng XQ, Wang PJ, Su L, et al. Sonographically guided microwave coagulation treatment of liver cancer: An experimental and clinical study. Am J Roentgenol 1998; 171: 449–454
- Huang J, Li T, Liu N, Chen M, He Z, Ma K, et al. Safety and reliability of hepatic radiofrequency ablation near the inferior vena cava: An experimental study. Int J Hyperthermia 2011; 27: 116–123
- Livraghi T, Goldberg SN, Lazzaroni S, Meloni F, Ierace T, Solbiati L, et al. Hepatocellular carcinoma: Radio-frequency ablation of medium and large lesions. Radiology 2000; 214: 761–768
- Rossi S, Distasi M, Buscarini E, Quaretti P, Garbagnati F, Squassante L, et al. Percutaneous RF interstitial thermal ablation in the treatment of hepatic cancer. Am J Roentgenol 1996; 167: 759–768
- Goldberg SN, Grassi CJ, Cardella JF, Charboneau JW, Dodd GD, III, Dupuy DE, et al. Image-guided tumor ablation: Standardization of terminology and reporting criteria. Radiology 2005; 235: 728–739
- Ren H, Liang P, Yu X, Wang Y, Lu T, Li X. Treatment of liver tumours adjacent to hepatic hilum with percutaneous microwave ablation combined with ethanol injection: A pilot study. Int J Hyperthermia 2011; 27: 249–254
- Livraghi T. Radiofrequency ablation of hepatocellular carcinoma. Surg Oncol Clin N Am 2011; 20: 281–299
- Lencioni R, Cioni D, Bartolozzi C. Percutaneous radiofrequency thermal ablation of liver malignancies: Techniques, indications, imaging findings, and clinical results. Abdom Imaging 2001; 26: 345–360
- Buscarini L, Buscarini E, Stasi MD, Vallisa D, Quaretti P, Rocca A. Percutaneous radiofrequency ablation of small hepatocellular carcinoma: Long-term results. Eur Radiol 2001; 11: 914–921
- Vogl TJ, Straub R, Eichler K, Woitaschek D, Mack MG. Malignant liver tumors treated with MR imaging-guided laser-induced thermotherapy: Experience with complications in 899 patients (2520 lesions). Radiology 2002; 225: 367–377
- Murakami R, Yoshimatsu S, Yamashita Y, Matsukawa T, Takahashi M, Sagara K. Treatment of hepatocellular carcinoma: Value of percutaneous microwave coagulation. Am J Roentgenol 1995; 164: 1159–1164
- Liang P, Dong B, Yu X, Yu D, Wang Y, Feng L, et al. Prognostic factors for survival in patients with hepatocellular carcinoma after percutaneous microwave ablation. Radiology 2005; 235: 299–307
- Dong B, Liang P, Yu X, Su L, Yu D, Cheng Z, et al. Percutaneous sonographically guided microwave coagulation therapy for hepatocellular carcinoma: Results in 234 patients. Am J Roentgenol 2003; 180: 1547–1555
- Okada S. Local ablation therapy for hepatocellular carcinoma. Semin Liver Dis 1999; 19: 323–328
- Kapoor BS, Hunter DW. Injection of subphrenic saline during radiofrequency ablation to minimize diaphragmatic injury. Cardiovasc Intervent Radiol 2003; 26: 302–304
- Raman SS, Aziz D, Chang X, Sayre J, Lassman C, Lu D. Minimizing diaphragmatic injury during radiofrequency ablation: Efficacy of intraabdominal carbon dioxide insufflation. Am J Roentgenol 2004; 183: 197–200
- Shao Q, Liang P, Zhang H, Shi W, Li X. Percutaneous microwave ablation of dog liver tissue abutting the diaphragm. Chin J Interv Imaging Ther 2010; 17: 314–319
- Solbiati L, Ierace T, Tonolini M, Osti V, Cova L. Radiofrequency thermal ablation of hepatic metastases. Eur J Ultrasound 2001; 13: 149–158
- Andromanakos N, Filippou D, Papadopoulos V, Kouraklis G, Chirstianakis E, Kostakis A. New concepts in the therapeutic options of liver metastases from colorectal cancer. J BUON 2007; 12: 445–452
- 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
- Goldberg SN, Gazelle GS, Mueller PR. Thermal ablation therapy for focal malignancies: A unified approach to underlying principles, techniques, and diagnostic imaging guidance. Am J Roentgenol 2000; 174: 323–331
- Koda M, Ueki M, Maeda N, Murawaki Y. Diaphragmatic perforation and hernia after hepatic radiofrequency ablation. Am J Roentgenol 2003; 180: 1561–1562
- Bilchik AJ, Wood TF, Allegra D, Tsioulias GJ, Chung M, Rose DM, et al. Cryosurgical ablation and radiofrequency ablation for unresectable hepatic malignant neoplasms: A proposed algorithm. Arch Surg 2000; 135: 657–662
- Raman SS, Lu DS, Vodopich DJ, Sayre J, Lassman C. Creation of radiofrequency lesions in a porcine model: Correlation with sonography CT, and histopathology. Am J Roentgenol 2000; 175: 1253–1258
- Brace CL. Microwave tissue ablation: Biophysics, technology, and applications. Crit Rev Biomed Eng 2010; 38: 65–78
- Garrean S, Hering J, Saied A, Hoopes PJ, Helton WS, Ryan TP, et al. Ultrasound monitoring of a novel microwave ablation (MWA) device in porcine liver: Lessons learned and phenomena observed on ablative effects near major intrahepatic vessels. J Gastrointest Surg 2009; 13: 334–340
- Bolser DC, Hobbs SF, Chandler MJ, Ammons WS, Brennan TJ, Foreman RD. Convergence of phrenic and cardiopulmonary spinal afferent information on cervical and thoracic spinothalamic tract neurons in the monkey: Implications for referred pain from the diaphragm and heart. J Neurophysiol 1991; 65: 1042–1054
- Head HW, Dodd GD, III, Dalrymple NC, Prasad SR, EI-Merhi FM, Freckleton MW, et al. Percutaneous radiofrequency ablation of hepatic tumors against the diaphragm: Frequency of diaphragmatic injury. Radiology 2007; 243: 877–884
- Kang TW, Rhim H, Kim EY, Kim YS, Choi D, Lee WJ, et al. Percutaneous radiofrequency ablation for the hepatocellular carcinoma abutting the diaphragm: Assessment of safety and therapeutic efficacy. Korean J Radiol 2009; 10: 34–42
- Ishigami K, Yoshimitsu K, Nishihara Y, Irie H, Asayama Y, Tajima T, et al. Hepatocellular carcinoma with a pseudocapsule on gadolinium-enhanced MR images: Correlation with histopathologic findings. Radiology 2009; 250: 435–443
- Xu W, Li JD, Shi G, Li JS, Dai Y, Wang XF. Different prognostic factors are associated with early and late intrahepatic recurrence following curative hepatectomy for patients with hepatocellular carcinoma. Zhonghua Wai Ke Za Zhi 2010; 48: 806–811