CT-Guided Percutaneous Microwave Ablation of Adrenal Malignant Carcinoma
Preliminary Results
Xin Li, MD; Weijun Fan, MD; Liang Zhang, MD; Ming Zhao, MD; Zilin Huang, MD; Wang Li, MD; Yangkui Gu, MD; Fei Gao, MD; Jinhua Huang, MD; Chuanxing Li, MD; Fujun Zhang, MD; and Peihong Wu, MD
BACKGROUND: Microwave ablation has recently been developed as a safe and effective treatment for a variety of tumors. The authors evaluated the safety and efficacy of computed tomography (CT)-guided percutaneous micro- wave ablation of adrenal malignant tumors. METHODS: Nine patients between 41 and 83 years of age (average age, 54 years) with adrenal carcinoma (a total of 10 lesions) received CT-guided percutaneous water-cooled microwave ablation. The 9 cases included 1 primary adrenocortical carcinoma and 8 metastatic carcinomas (4 from lung cancer, 2 from hepatocellular carcinoma, 1 from intrahepatic cholangiocarcinoma, and 1 from left tibial osteosarcoma). Of the 8 metastatic cases, 7 were unilateral, and 1 was bilateral. All cases were pathologically con- firmed by aspiration biopsy or postsurgical biopsy. The tumor diameters ranged from 2.1 cm to 6.1 cm (average, 3.8 cm). The average number of ablation sites was 1.5 sites (1-3 sites), and the average accumulated ablation time was 7.7 minutes (4-15 minutes). The procedures were performed using a cooled-shaft antenna. RESULTS: The patients were followed for 3-37 months, with an average of 11.3 months. Nine of 10 lesions were completely necro- tized after first treatment. The other lesion was completely necrotized after 2 treatments. One of the patients expe- rienced hypertensive crisis during treatment. No patient experienced recurrent tumor at the treated site, and this lack of recurrence indicated effective local control. All patients had progression of metastatic disease at extra- adrenal sites. CONCLUSIONS: CT-guided percutaneous water-cooled microwave ablation is a minimally invasive and effective method for the treatment of adrenal carcinoma. Cancer 2011;117:5182-8. @ 2011 American Cancer Society.
KEYWORDS: adrenal, malignant carcinoma, microwave, ablation, therapeutic effect.
Adrenal malignant tumors comprise many pathological tumor types including primary and metastatic tumors. The majority of primary adrenal carcinomas are adrenocortical carcinoma and malignant pheochromocytoma. Most metastatic tumors to the adrenal gland arise from lung cancer, followed by renal carcinoma, melanoma, and gastroin- testinal cancer.1-3 Abdominal surgery and laparoscopic excision are the traditional treatments for primary adrenal car- cinoma.4-8 Although controversial, surgical excision of isolated adrenal metastatic tumors has been supported by some researchers.719 Recently, an increasing number of minimally invasive treatments, such as selective arterial emboliza- tion, radiofrequency ablation, chemical ablation, laser ablation, and microwave ablation, have been used to treat adre- nal carcinoma. 10-16
Microwave ablation has been developed in the current decade as a new tumor ablation technique and is widely used to treat many types of malignant carcinomas including liver cancer, lung cancer, metastatic bone tumors, and renal tumors.16-20 Microwave ablation of the adrenal gland is a promising technique for percutaneous treatment of adrenal malignant tumors, although there is limited experience reported in the literature.16,21,22 We retrospectively analyzed patients with adrenal carcinomas who underwent microwave ablation in our department with the goal to evaluate the safety, practicality, and efficacy of CT-guided microwave ablation of adrenal carcinomas.
Corresponding author: Weijun Fan, MD, or Pei Hong Wu, MD, 651 Dongfeng Road, East, Guangzhou, Guangdong 510060, PRC; fanweijun1964@126.com or peihongwu1956@tom.com
Department of Medical Imaging and Interventional Radiology, Cancer Center and State Key Laboratory of Oncology in South China, Sun Yat Sen University, Guangzhou, China
DOI: 10.1002/cncr.26128, Received: November 2, 2010; Revised: January 19, 2011; Accepted: February 17, 2011, Published online April 26, 2011 in Wiley Online Library (wileyonlinelibrary.com)
| Patient No. | Tumor Location | Pathology | Tumor Diameter | No. of Ablation Sites | Power Setting | Accumulated Ablation Time, min |
|---|---|---|---|---|---|---|
| 1 | Right | Tibial osteosarcoma | 4.0 × 2.5 | 1 | 70 | 8 |
| 2ª | Left | Adrenocortical carcinoma | 6.1 × 3.8 | 3 | 70 | 15 |
| 3 | Left | Lung adenocarcinoma | 2.9 × 2.0 | 1 | 60 | 5 |
| 4 | Right | Large cell lung carcinoma | 4.1 × 3.9 | 2 | 50 | 10 |
| 4 | Left | Large cell lung carcinoma | 3.6 × 2.5 | 1 | 60 | 7 |
| 5 | Left | Hepatocellular carcinoma | 3.5 × 3.3 | 2 | 70 | 8 |
| 6 | Right | Cholangiocarcinoma | 3.6 × 1.8 | 1 | 60 | 6 |
| 7 | Left | Hepatocellular carcinoma | 2.1 × 2.0 | 1 | 50 | 4 |
| 8 | Right | Pulmonary squamous cell carcinoma | 5.2 × 4.2 | 2 | 70 | 10 |
| 9 | Right | Lung adenocarcinoma | 2.7 × 2.2 | 1 | 60 | 4 |
a At 1-month follow-up, computed tomography (CT) showed residual tumor. Thus, a second microwave ablation (50 W, 5 min) was performed. One month after the second ablation, follow-up showed complete tumor necrosis.
MATERIALS AND METHODS
Patients
Patient data
This retrospective study was approved by our inter- nal review board. Before treatment, all patients received a detailed explanation of the ablation procedure, possible complications, and expected outcomes. All patients gave their written informed consent before treatment. From July 2007 to June 2010, 9 patients (8 men and 1 woman between 41 and 83 years of age; average age, 54 years) received CT-guided microwave ablation of adrenal solid tumors at our hospital. Some tumors were not operable because of other coexisting diseases, and some patients refused surgical excision. One patient a had recurrence after a surgical resection, and the tumor was not removed in a second surgical excision.
Tumor characteristics
A total of 10 lesions received ablation treatment. Five were located within the left adrenal gland, and 5 were located within the right adrenal gland. The diameters of the lesions ranged from 2.1 cm to 6.1 cm, with an average of 3.8 cm. Nine of the 10 lesions were pathologically con- firmed by CT-guided fine-needle aspiration biopsy, and the other was pathologically confirmed after surgical exci- sion. One lesion was a primary adrenocortical carcinoma, and the other 9 were metastatic adrenal carcinomas (5 from lung cancer, 2 from hepatocellular carcinoma, 1 from intrahepatic cholangiocarcinoma, and 1 from left tibial osteosarcoma; See Table 1). Before ablation, all met- astatic carcinomas were isolated adrenal metastasis, and their primary tumors were all controlled by chemother- apy, microwave ablation, or surgical excision.
Preparation before the ablation
All patients received complete routine laboratory examinations, including complete blood count (CBC), blood chemistry, viral titers (such as hepatitis B virus [HBV], hepatitis C virus [HCV], and human immunodefi- ciency virus [HIV]), and coagulation profile examinations.
Methods
All ablations were performed with intravenous conscious sedation. The patients’ vital signs were continuously monitored, especially changes in blood pressure. The blood pressure measurement was performed every 5 minutes, and its frequency was increased to every 3 minutes after the start of ablation. When the patient expe- rienced intolerable pain during the ablation, 100 mg tra- madol hydrochloride (Grunenthal, Aachen, Germany) was injected intravenously for pain relief.
Imaging guidance
Treatment of all 10 tumors was performed under CT guidance. CT was performed using the Picker CT-Twin Flash scanner (Elscint, Haifa, Israel). The adrenal gland was scanned at 120 kV, 275 mA, using a slice thickness of approx- imately 3-5 mm, and a pitch of 1. Except for 1 patient in the supine position (Fig. 1), other patients were scanned in a lat- eral or prone position before the ablation. After adrenal gland CT scanning, appropriate scanned layers were selected, and the puncture angles and depths were thereby confirmed.
Surgical technique
Local anesthesia was given at the selected puncture points with 2% lidocaine. After a surgical incision was made, the 14-gauge microwave antenna was inserted into the tumor at a predetermined angle in a stepwise manner.
a.
b.
c.
CT scanning was performed, again, to ensure that the
ablation antenna had been placed in the appropriate posi-
tion within the tumor. For microwave ablation, we used a
commercially available system (FORSEA; Qinghai
Microwave Electronic Institute, Nanjing, China) and a
14-gauge cooled-shaft antenna. Internal cooling of the
antenna shaft was performed with a peristaltic pump
(BT01-100 LanGe-Pump; LanGe Steady Flow Pump,
Baoding, China) that recirculated chilled saline solution
(5060 mL/min) to maintain a mean shaft temperature
of 10°C ± 2 (standard deviation). The power was gener-
ally set at approximately 50-70 W. The ablation time for
24 cm tumors was 410 minutes. For tumors larger
than 4 cm, ablation was performed with multiple-site
superposition, or using an appropriately elongated treat-
ment time, depending on our previous ablation experi-
ence with other solid tumors such as liver, with the aim to
completely necrotize the tumor. Nine of the 10 tumors
were treated in 1 session, whereas the remaining tumor
was treated with a second ablation because of tumor resid-
uals (Table 1). We used 13 ablation sites per lesion (av-
erage, 1.5 sites), with an accumulated ablation time which
ranged from 4 to 15 minutes (average, 7.7 minutes). After
ablation, track ablation was performed to avoid implanta-
tion metastasis in the probe’s pathway. All operations
were completed by 1 of the 4 interventional radiologists
(Fan Wei Jun, Zhang Liang, Zhao Ming, and Huang Zi
Lin), all of whom had more than 10 years of experience in
tumor ablation. Following treatment, CT scanning was
again performed to evaluate the immediate necrotic con-
ditions after ablation and to examine whether there were
any complications, such as bleeding.
Patient Follow-Up
After treatment, all patients received continuous electro- cardiogram (ECG) and pain monitoring for 4 hours in the recovery ward. When a patient experienced pain, anal- gesic treatment was given. All patients were discharged af- ter 2 days of observation.
We followed all treated patients. A dual-phase CT- enhanced scan, an arterial phase lasting 35 seconds and a venous phase lasting 60 seconds, was performed 1 month after treatment to evaluate the degree of tumor necrosis (no enhancement indicating complete tumor necrosis, areas of enhancement indicating possible residual tu- mor) and to observe for new areas of enhancement in the adrenal gland (indicating tumor relapse). All examina- tions were performed with a spiral CT scanner
a.
b.
..
/
c.
d.
(Brilliance 16; Philips, Amsterdam, the Netherlands) using a sequential acquisition of 5 mm-thick sections, 120 kV, and 250 mA. Iohexol (Omnipaque 240; Amersham Health, Princeton, NJ), at an injection speed of 3 mL/s, was used as the contrast agent. Subsequent CT examina- tions were performed in the third month after treatment and every 6 months afterwards, or depending on clinical conditions.
Two of the authors (Li Xin and Zhang Liang) were in charge of collecting follow-up data, including the level of tumor necrosis, the existence of residual tumor, tumor recurrence, new metastasis, progression of the primary tumor, and the overall condition (such as survival) of each patient. The data were acquired using CT scanning, direct patient contact, or review of medical records stored in the medical records room of our hospital.
RESULTS
Clinical Evaluation of the Therapeutic Effects and Patient Follow-Up
The average follow-up period was 11.3 months (aver- age, 3~37 months). Nine of the 10 tumors were com- pletely necrotized after first ablation, which included 1 patient with a bilateral adrenal metastasis (Fig. 2). Af- ter microwave ablation of the bilateral adrenal tumors, the patient received substitutive treatment with oral glucocorticoid and fludrocortisones. Only 1 lesion showed residual tumor at 1-month follow-up. After the second ablation, the tumor was completely necro- tized, as revealed by enhanced CT at 1-month follow- up (Fig. 3). However, subsequent visits found lung and liver metastasis in the patient. Five of the 8 patients with adrenal metastatic tumors died from the
a.
b.
0
c.
d.
progression of their primary tumors or its metastasis to other organs.
Adverse Reactions and Complications
One patient experienced a hypertensive crisis. This patient, aged 50 years, had right-sided lung cancer accom- panied by an isolated left adrenal gland metastasis. He had no previous hypertensive history with a baseline blood pressure of 136/85 mm Hg. The adrenal tumor was 2.9 cm × 2.0 cm in size. One minute after the start of abla- tion, the patient experienced a sudden spike in blood pres- sure to 243/147 mmHg accompanied by headache, tachycardia, and ventricular arrhythmia. The ablation was immediately paused, and the patient received an intrave- nous injection of 5 mg phentolamine mesylate (Regitine;
Nycomed, Zurich, Switzerland). His blood pressure returned to baseline 5 minutes after the injection. To completely remove the tumor, microwave ablation was resumed. However, the patient again experienced a similar high blood pressure reaction. The crisis was controlled again with another 5 mg Regitine injection. Afterwards, the patient remained stable to the end of ablation. After the procedure, the patent received continuous ECG mon- itoring for 4 hours, and the blood pressure remained at baseline. In subsequent follow-ups, no obvious nervous or cardiopulmonary complications were noted.
Another patient experienced pain after returning to the recovery ward. Oral paracetamol tablets (Sino-Ameri- can Shanghai Squibb Pharmaceuticals, Shanghai, China) were given, but the pain persisted. Afterward, the patient
received an intramuscular injection of tramadol hydro- chloride, which relieved the pain. No complications were reported by the other patients.
DISCUSSION
The use of image-guided heat ablation (including radio- frequency, microwave, and laser ablation) has been widely applied to all types of solid tumors as a minimally invasive treatment method. Compared with radiofrequency abla- tion, microwave ablation has the following advantages: continuous higher intratumoral temperatures, faster temperature rise rate, larger ablation volume, and shorter ablation time.16,23-26 In addition, due to the inherent non- electrical properties of the electromagnetic waves, the microwave ablation device requires no external electrodes; thus, the risk of burning caused by external electrodes used in radiofrequency ablation is avoided.16 Furthermore, ra- diofrequency ablation fails to adequately heat cystic tumors. The cystic characteristics of adrenal metastatic tumors are more amenable to microwave ablation.16
Our preliminary results showed that microwave
ablation was able to effectively destroy both primary and
metastatic adrenal carcinomas. Similar to our results,
Wang et al21 performed ultrasound-guided ablations on 5
unilateral adrenal metastatic tumors of 2.34.5 cm in di-
ameter, at 12 sites per lesion. The researchers found no
residual tumor at the ablation locations at approximately
8-31 months of follow-up. Our study differed from the
above study by the finding that 1 of the tumors we treated
presented with residual tumor. The remaining tumor had
enlarged to 6.1 cm in diameter and completely necrotized
after a second microwave ablation. Mayo-Smith et al
reported that after radiofrequency ablation, 2 of the 13
cases with adrenal tumors, which averaged more than 6
cm in diameter, showed residual tumor. These results of
heat ablation showed that when the tumor’s diameter
exceeded 5 cm, a complete tumor ablation rate was less
than 30%, despite multiple-site repeated ablation.27,28
Therefore, adrenal malignant tumors larger than 5 cm
had a greater possibility of residual tumor or relapse after
microwave ablation. Regular and timely follow-ups are
necessary. Secondary microwave ablation should be per-
formed on areas with relapse or residual tumor.
In this study, complications including pain and hy- pertensive crisis were controlled by corresponding inter- ventions. Due to its higher potential death rate, hypertensive crisis is a critical complication of microwave ablation. Onik et al29 reported 2 patients with intrahe-
patic metastatic tumor located near the normal right adre- nal gland who experienced hypertensive crisis during radiofrequency ablation. One of the 2 patients showed a prominent rise in the catechol level, 10 times higher than normal. The catechol level returned to normal after treat- ment. Chini et al30 reported the first case of hypertensive crisis that resulted from ablation of adrenal metastatic tu- mor. In our study, 1 patient also demonstrated hyperten- sive crisis. To our knowledge, this is the first report of a hypertensive crisis caused directly by microwave ablation of adrenal tumor. Some researchers suggest that as micro- wave ablation elevates the temperature more rapidly than radiofrequency ablation, it is more likely to induce hyper- tensive crisis.16 However, compared with radiofrequency ablation, microwave ablation requires less time to treat a tumor due to its faster temperature rise rate. This reduces the stimulation to the adrenal gland and the subsequent occurrence of hypertensive crisis. Long-term, randomized, controlled studies are required to determine whether microwave or radiofrequency ablation has a higher tend- ency to induce hypertensive crisis. In light of potential hypertensive crises, vital signs (especially changes in blood pressure) should be closely monitored during ablation of adrenal tumors, particularly tumors with endocrine func- tion. In case of hypertensive crisis, a-blockers or ß-block- ers are the 2 main treatment options. 12,
Our study had several limitations. Although our pre- liminary results showed that microwave ablation resulted in excellent local control rates over adrenal carcinomas, selection of appropriate candidates for microwave ablation is crucial to accurately evaluate the therapeutic effects. In our study, all adrenal metastatic tumor patients showed progression of their original tumors or metastasis outside the adrenal gland. The patients with primary adrenocortical carcinoma developed lung and liver metastasis. These pro- gressions had a crucial impact on the prognosis. Due to our small sample size and short follow-up period, we could not assess whether local ablation of adrenal tumors contributed to overall patient survival. Future studies on ablation not only should be conducted on a larger sample size, but they should be compared against surgical resection in a prospec- tive, randomized, controlled design. Patients who received microwave ablation of adrenal tumors should be contrasted with those who received surgical resection in terms of pro- gression-free survival, recurrence rates, complication rates (including hypertensive crisis), and 1-5 year survival. Meanwhile, factors affecting the prognostic outcomes fol- lowing microwave ablation on adrenal carcinomas should also be analyzed. We hope that through such future studies,
the benefits of microwave ablation for patients with adrenal carcinomas can be verified.
CT allows precise measurements on the angles and depths of needle entry and provides direct visualization on the locations of adrenal tumors and the antenna. Thus, CT is the imaging tool of choice for guidance of micro- wave ablation of adrenal tumors.
Our preliminary results showed that microwave ablation exerts a definite local control rate on adrenal ma- lignant tumors. However, continued follow-up of patients is necessary to determine the long-term efficacy, sequelae, and appropriate patient selection criteria.
FUNDING SOURCES
No specific funding was disclosed.
CONFLICT OF INTEREST DISCLOSURES
The authors indicated no conflicts of interest.
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