ELSEVIER
EJR EUROPEAN JOURNAL OF RADIOLOGY
Percutaneous laser ablation of unresectable primary and metastatic adrenocortical carcinoma
Claudio M. Pacella*, Roberto Stasi, Giancarlo Bizzarri, Sara Pacella, Filomena Maria Graziano, Rinaldo Guglielmi, Enrico Papini
Regina Apostolorum Hospital, Department of Diagnostic Imaging and Interventional Radiology, Via San Francesco 50, Albano Laziale, Rome 00041, Italy
Received 2 December 2006; received in revised form 4 April 2007; accepted 5 April 2007
Abstract
Purpose: To evaluate the feasibility, safety, and clinical benefits of percutaneous laser ablation (PLA) in patients with unresectable primary and metastatic adrenocortical carcinoma (ACC).
Patients and methods: Four patients with hepatic metastases from ACC and a Cushing’s syndrome underwent ultrasound-guided PLA. In one case the procedure was performed also on the primary tumor.
Results: After three sessions of PLA, the primary tumor of 15 cm was ablated by 75%. After 1-4 (median 1) sessions of PLA, five liver metastases ranging from 2 to 5 cm were completely ablated, while the sixth tumor of 12 cm was ablated by 75%. There were no major complications. Treatment resulted in an improvement of performance status and a reduction of the daily dosage of mitotane in all patients. The three patients with liver metastases presented a marked decrease of 24-h urine cortisol levels, an improved control of hypertension and a mean weight loss of 2.8 kg. After a median follow-up after PLA of 27.0 months (range, 9-48 months), two patients have died of tumor progression, while two other patients remain alive and free of disease.
Conclusions: Percutaneous laser ablation is a feasible, safe and well tolerated procedure for the palliative treatment of unresectable primary and metastatic ACC. Further study is required to evaluate the impact of PLA on survival.
@ 2007 Elsevier Ireland Ltd. All rights reserved.
Keywords: Adrenocortical carcinoma; Metastases; Percutaneous laser ablation
1. Introduction
Adrenocortical carcinoma (ACC) is a rare malignancy, with an estimated incidence of one case per million per year [1]. It is slightly more common in women than men and is most commonly detected in the fifth decade [2]. At the time of pre- sentation, 30-40% of patients have clear evidence for metastatic disease [2,3]. Of the approximately 60% of tumors that present with a secretory syndrome, a mixed Cushing’s syndrome and vir- ilization caused by cosecretion of cortisol and adrenal androgens is most common (35%), followed by pure Cushing’s syndrome (30%) and pure virilization (20%). Aldosterone-secreting ACCs are rarely encountered (2%) [2].
Patients with ACC have limited treatment options [4]. Surgery remains the mainstay for primary and recurrent dis- ease. Repeated surgical resection is used in selected patients and is associated with long-term survival [5-7]. For patients who are not candidates for surgical resection, due to extent or distribution of disease or concurrent medical disability, or for whom the proven benefits of surgery do not outweigh the risks, other forms of cytoreductive therapy are warranted.
In recent years interest has focused on minimally invasive procedures as an alternative to surgery. Techniques such as per- cutaneous laser ablation (PLA) or radiofrequency ablation (RF) have been shown to produce local tissue destruction in a rapid, predictable, and inexpensive manner with minimal morbidity and a short recovery time [8]. They have been applied safely and effectively to a range of malignant primary and metastatic liver tumors, and both benign and malignant tumors of other organs [9]. However, the experience with ACC is very limited, due to the rarity of this tumor.
* Corresponding author. Tel .: +39 06 9329 8300; fax: +39 06 9329 8342. E-mail address: claudiomaurizio.pacella@fastwebnet.it (C.M. Pacella).
In this report we describe the use of PLA for the treatment of four patients with unresectable ACC. Our goal was to evaluate the feasibility, safety, and clinical benefits of this new treatment modality.
2. Patients and methods
2.1. Patients
Patients’ characteristics at the time of PLA are illustrated in Table 1. The primary adrenal tumor in case 1 had not been resected due to widespread metastatic disease and poor general conditions. In all patients the debulking procedure was requested as a palliative treatment to revert the progressive increase of cortisol levels, unresponsive to a high-dose mitotane treatment that induced severe gastrointestinal symptoms.
Liver metastases had been considered unresectable, either because of their number or location, or because of the extent of extrahepatic disease (Table 1). Tumor volume of the lesions and volume of coagulation necrosis were calculated on the basis of measurements in three dimensions. The three largest perpendic- ular diameters (referred as x, y, and z) were then used to calculate the volume of the images as an ellipsoid [(47/3) (x/2) (y/2) (z/2)].
Chemotherapy, consisting of mitotane, had been given to all patients until disease progression. Mitotane was started 1-3 months before laser treatment and given at doses of 4-8 g/day, with dose adjustments guided by the monitoring of plasma levels of the drug (therapeutic range: 14-20 µg/ml).
Treatment of patients was approved by the local institutional review board and a written informed consent was obtained from all patients.
2.2. Percutaneous laser ablation treatment
The procedure was performed under conscious sedation on liver metastases irrespective of their location (more specifically, we also included liver metastases supercially located or located less than 1 cm away from vital structures) and, in one case, on
the primary tumor following the method reported in detail else- where [10]. Neodymium: Yttrium Aluminium Garnet (Nd: YAG) laser operating at the wavelength of 1064 nm and plane-cut tip optical fibers with a quartz core of 300 mm were used (D.E.K.A .- M.E.L.A .; Florence, Italy). This laser source was used with an optical beam-splitting device (SMART 1064 HCC; D.E.K.A .- M.E.L.A., Florence, Italy) with four separate fibers that were always activated concurrently (simultaneous or multiple-fiber application). Four 21-gauge needles were positioned under ultra- sound guidance in the area to be treated in a square configuration of 1.5-2.0 cm per side. The needles were positioned one at a time through the single skin entry port. The optical fiber was inserted through each needle to the end of the sheath, which was then retracted, exposing at least 1.0 cm of bare tip in direct contact with the lesion. Whenever technically feasible, fibers were posi- tioned central into the tumor mass. For each illumination the laser was turned on at a power of 5.0 W with an exposure time of 360 s (1800 J per fiber) and 7200J (1800 × 4) was given in total with four fibers. One laser illumination lasting 6 min was considered a single tumor ablation. In case of liver metastases ≤5 cm up to two ablations (the first one carried out in the deepest part of the lesion, the second after pulling back the needles and the fiber tips 1.5-2.0 cm) was performed during a single session (a single intervention that consisted of one or more ablations per- formed on one or more tumors) with the intention to destroy the entire tumor plus a 0.5-1.0 cm “cuff” of adjacent normal liver. The cuff of normal liver is destroyed in an attempt to create a tumor-free margin. Up to three illuminations were performed during a single session in the liver metastases >5 cm (overlap- ping ablation). The risks of collateral damage to adjacent normal tissues were substantially minimized thanks to continuous imag- ing throughout the procedure, which also allowed modification of the delivered therapy to optimize therapeutic outcomes.
2.3. Efficacy and safety evaluations
An abdominal CT scan was performed 24-48 h after each PLA session to assess the extent of treatment-induced coagu-
| Case 1 | Case 2 | Case 3 | Case 4 | |
|---|---|---|---|---|
| Sex | F | M | M | F |
| Age (years) | 53 | 49 | 59 | 54 |
| Previous adrenalectomy | No | Yes | Yes | Yes |
| Recurrence in adrenal bed | Not applicable | No | No | Yes |
| Time between diagnosis of ACC and the development of any metastases (mos) | 0ª | 0ª | 44 | 36 |
| Site and number of metastases | Liver (n=11), lungs (n=8), lymph nodes (n=5), skeleton (n=3) | Liver (n=1), lungs (n=3) | Liver (n=1), lungs (n=3) | Liver (n=3) |
| Number of liver metastases | 11 | 1 | 1 | 3 |
| Reason for unresectability | Extrahepatic disease and poor general condition | Extrahepatic disease | Extrahepatic disease | Number/location disease of lesions |
| Cushing's syndrome | Yes | Yes | Yes | Yes |
| Chemotherapy with mitotane | Yes | Yes | Yes | Yes |
a Metastatic disease at the time of initial diagnosis.
lation necrosis. Areas of hypoattenuation that did not enhance with contrast medium were considered to represent necrotic tis- sue. In these cases, the efficacy of PLA had to be confirmed by a CT scan at 3 months. For cases with incomplete necrosis, an additional PLA session was scheduled within 2 weeks of the first one. Initial treatment failure was defined as the presence of viable tumor at the end of treatment.
The reporting standards of the International Working Group on Image-Guided Tumor Ablation were adopted [11]. A com- plete response was defined as disappearance of the tumor, confirmed by the absence of contrast-enhancing tissue. For patients with residual disease undergoing chemotherapy, sta- ble disease was defined as a reduction of less than 50% in the area of all measurable lesions, or an increase of less than 25%. Tumor progression was defined as an increase of at least 25% in the overall area of the tumor or appearance of new lesions [11,12].
Follow-up, Karnofsky score and outcome were documented by subsequent clinical visits with hormonal and metabolic pro- files, and chest and abdominal CT every 3-6 months according to clinical need. Additional tests were performed as required by the clinical evaluation of the patients.
Complications and side effects of treatment were described using the reporting standards of the Society of Interventional Radiology [13].
2.4. Statistical analysis
Continuous variables were summarized by descriptive statis- tics. Categorical variables were summarized by frequency statistics. Means and standard deviations (S.D.s) of continuous variables and frequencies and proportions of discrete variables are reported. Changes in hormonal levels and Karnofsky score from baseline were compared using t-test for dependent samples. All P values are two-tailed.
3. Results
3.1. Treatment efficacy
Tumor characteristics and results of treatment of liver metas- tases are summarized in Table 2. The single primary adrenal tumor that we treated originated from the left adrenal gland of case 1. It had a maximum volume of 1080 ml (Fig. 1a and b). We performed a total 9 illuminations in 3 sessions (three illuminations per a single session). Treatment was then discon- tinued because of the evidence of progression of disease at both extraadrenal and extrahepatic sites.
Liver metastases had a volume ranging from 4 to 567 ml. We performed a total of 22 illuminations during 10 PLA ses- sions. The total median number of sessions per liver metastasis was 1 (range 1-4, mean 1.6) and, the total median number of illuminations per liver metastasis was 2 (range 1-11, mean 3.6). In liver metastases ≤5.0 cm (cases 1, 2 and 4) the median number of sessions was 1 (range 1-2, mean 1.6) and, median number of illuminations was 2 (range 1-2, mean 1.3). In liver metastasis >5.0 cm (case 3) we performed 11 illuminations in 4
| Patient | Previous adrenalectomy | Number of liver mets treated/overall number of liver mets | Liver segments (cm) involved | Tumor size (cm) | Number of PLA illumination/number of sessions (energy delivered) | Local tumor control % necrosis | Size of necrosis (cm) | Local recurrence (mos) | New lesions (mos) | Disease (mos) free-survival | Survival (mos) from PLA |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Case 1 | No | 12.0 × 12.0×15.0 | 9/3 (64,800) | 75% | 12.0 × 11.5×12.0 | ||||||
| 1/11 | S4ª | 4.5× 4.5×3.8 | 2/1 (14,400 J) | 100 | 5.0 × 5.5×5.5 | 9 | |||||
| Case 2 | Yes | 1/1 | S6 | 2.0× 1.8×2.0 | 1/1 (7200 J) | 100 | 3.0 × 3.5×3.0 | 4b | 28+ | ||
| Case 3 | Yes | 1/1 | S6,7,8,5 | 7.5 × 12.6×12.0 | 11/4 (79,200J) | 75€ | 7.0× 13.0×10.0 | 23 | |||
| Case 4 | Yes | 3/3 | S7d | 3.5 × 3.0×3.0 | 2/1 (14,400 J) | 100 | 4.0 ×4.0×3.5 | 35 | 13 | 48+ | |
| S8 | 4.5 × 4.2×4.0 | 4/2 (28,800 J) | 80€ | 5.0 × 5.0×6.0 | 19-24 | ||||||
| S6ª | 3.5 × 3.0×3.2 | 2/1 (14,400 J) | 100 | 4.5×3.5×4.0 |
a Beneath the capsule of the liver.
b This patient underwent surgery for removal of the lung metastasis.
” After the first four sessions.
d Adjacent to inferior vena cava.
e After one session with the size of necrosis of 4.0 x 4.0 x 3.8.
(a)
(b)
sessions (three illuminations in the first three sessions and two illuminations in the fourth).
After PLA, 5 liver metastases with a diameter ≤5.0 cm were ablated completely (Fig. 2), and 1 (case 3) with a diameter of 12 cm was ablated by 75%. A complete response (disappearance of all liver metastases) was observed in two cases (case 2 and 4).
In the patient with unresected primary tumor (case 1) several liver metastases were present in different segments of the liver. Only the largest liver metastasis with diameter <5 cm was treated and ablated completely with PLA. Again, PLA treatment was interrupted due to progressive extrahepatic disease.
In the three patients with liver metastases, repeat determi- nation of hormonal levels revealed a reduction of free urine cortisol from a mean baseline value of 396 µg/24-h to 93 µg/24- h after the end of treatments, and a moderate increase of plasma ACTH levels from a mean baseline value of 3.5 pg/ml to a post-treatment value 28.4 pg/ml. The patient with unresectable primary tumor showed only a slight reduction of 24-h urine free cortisol but PLA made possible to decrease the ill-tolerated mitotane dosage (from 8.0 to 4.5 g/day) with the subse-
(a)
(b)
quent improvement of nausea, vomiting, diarrhea and muscle tremors.
All patients showed an improvement of their clinical con- ditions as indicated by a higher Karnofsky score (P=0.010; Table 3). This improvement was maintained for a 6 months in case 1 and 5 months in case 3, who died of progressive dis- ease, whereas the two other patients have remained alive and free of disease. Additional details about patients’ follow-up are reported in Table 2.
3.2. Treatment safety
We observed only side effects classified as Class B accord- ing to the reporting standards of the Society of Interventional Radiology [13]. Abdominal pain induced by PLA occurred in three cases (case 1, 3 and 4) and was controlled during the 24 h following the procedure with the parenteral administration of ketoprofen. Other side effects were pleural effusion in one patient (case 4) and an increase in body temperature ≤38.5℃ in three patients (case 1, 3 and 4). All patients were discharged or were free of procedure-related medical care 48 h after the PLA sessions without major complications. The patient in whom the adrenal tumor was treated did not show a worsening of his hypertensive state during or after the procedure.
| Plasma ACTH (pg/ml) | Serum cortisol levels (µg/dl) | 24-h urine free cortisol (pg) | DHEAS (mg/ml) | Karnofsky score (%) | Mitotane | |
|---|---|---|---|---|---|---|
| Case 1 | ||||||
| Baseline | 2 | 467 | 650 | 2207 | 35 | 6000 |
| After the 1st treatment | 0.98 | 276 | 647 | ND | 50 | |
| After the 2nd treatment | ND | ND | ND | ND | 70 | 3000 |
| 3 months after the last treatment | 4.6 | 399 | 550 | 1520 | 60 | 2500 |
| Case 2 | ||||||
| Baseline | 2.7 | 565 | 638 | 1950 | 35 | 4000 |
| After the 1st treatment | 10 | 627 | 50 | ND | 70 | |
| After the 2nd treatment | 18 | 396 | 337 | ND | 70 | 3500 |
| 3 months after the last treatment | 30 | 847 | 147 | 920 | 60 | 2000 |
| Case 3 | ||||||
| Baseline | 3 | 304 | 251 | 8684 | 70 | 8000 |
| After the 1st treatment | 20 | 278 | 72 | ND | 80 | 4500 |
| 3 months after the last treatment | 9.3 | 79 | 45 | 4249 | 90 | 4000 |
| Case 4 | ||||||
| Baseline | 5 | 195 | 300 | 1736 | 70 | 4000 |
| After the 1st treatment | 30 | 199 | 88 | ND | 80 | |
| After the 2nd treatment | 35 | 188 | 90 | ND | 80 | 2500 |
| 3 months after the last treatment | 46 | 174 | 89 | 275 | 80 | 2000 |
| P* | ns | ns | ns | ns | 0.010 | 0.02 |
Normal ranges: plasma ACTH, 9-52 pg/ml; serum cortisol (8.00 a.m.), 50-250 µg/dl; 24-h urine free cortisol, 20-90 µg; serum DHEAS, adult: 1200-3600, menopause: 100-800 ng/ml. ND = not done.
* The P value was calculated between the first and the last value.
4. Discussion
This is the first study to evaluate the use of PLA for the management of unresectable ACC. Our findings corrob- orate previous studies showing that PLA can be performed safely in patients with tumors of solid abdominal organs [8,9]. Ultrasound-guidance was preferred to CT-guidance because in our experience the former is easier to use, even for lesions under the diaphragm or near the bowels. In fact, US-guidance allows real-time targeting of the fiber tips in the area to be treated and is less time-consuming than CT-guidance. The laser source with a beam splitter allows four different fibers to be advanced into the tumor in any geometry desired by the operator. Multiple punctures with smaller-gauge needles allow applica- tion of laser fibers in a geometric arrangement that fits tumor morphology better, particularly in irregular-shaped tumors and difficult locations near the diaphragm, biliary tree or the infe- rior vena cava. The use of fine needles and US-guidance allows a more flexible and safe approach even through the intercostal route. The extent of coagulation necrosis cannot be predicted from mathematical models because of the complex interac- tions between laser light and tumor tissue [14], highlighting the importance of accurate real-time monitoring of necrosis. Small lesions (with diameter ≤5 cm) were more easily eradicated than larger lesions, in accordance with other studies [15]. Regard- ing local tumor control, we observed recurrences in two cases. The PLA technique that we adopted produced few and easily manageable minor treatment-related adverse events. We did not observe abscess formation, intraabdominal bleeding, or visceral injury.
Feasibility, safety, and good response rate by themselves are necessary but not sufficient conditions to make these techniques useful in the clinical setting. Although patients with metastatic ACC have limited therapeutic options, a crucial point about any new treatment is whether it results in any advantage to the patient. With all the limitations of a preliminary report, our results suggest that the cases we have treated may have received a clinical benefit from this procedure. We are aware that the concurrent use of mitotane prevents drawing conclusions on the long-term data, but it is noteworthy that PLA treatments resulted in a rapid improvement of patients’ performance status associ- ated with the decrease of the daily dosage of mitotane. This is particularly encouraging in consideration of the fact that in several series medical therapy with mitotane in patients with unresectable tumors appeared to be of little benefit, with median survivals of 3-9 months [3].
Percutaneous ablation techniques different from ours have been described for the treatment of adrenal tumors. Vogl et al. have used laser-induced interstitial thermotherapy (LITT) to treat nine patients with adrenal metastases [16]. The LITT pro- cedure requires CT guidance to position an irrigated power laser application system. Small lesions (≤1 cm) are treated with one laser applicator system; for larger lesions (>1 cm) up to four laser application systems are inserted so that larger areas of coagula- tion necrosis can be obtained. This is calculated according to the maximum distance of 20 mm for the position of the laser applica- tors next to each other. The actual LITT treatment is performed under MR guidance using T1-weighted gradient echo sequences. The laser application is stopped after coagulation of the lesion has been confirmed in the MR images. This allows complete
tumor ablation plus a variable tumor margin to be created in a more controlled and reproducible fashion compared to the hyperechoic focus that is formed when performing RF and LA with US guidance. Contrast-enhanced T1-weighted sequences are subsequently performed to visualize the immediate effect of the ablation and the actual formation of an ablation zone. Com- plete ablation with this technique was achieved in seven lesions with local tumor control rate equal to 78%, with no complica- tions occurring during and after the laser treatments. Vogl et al. obtained in liver metastases from colorectal cancer a local tumor control between 96.3% and 98.8% after 3 months and 95.6% and 98.8% after 6 months after LITT. No local recurrence was observed later than 6 months after LITT. These excellent results show that the clinical advantages of MR monitoring are quite relevant and that the clinical advantages of US targeting is as much as important but is counteracted by the difficulties of US real-time monitoring. However, it should be pointed out that US-guided procedures are by far less expensive and more widely available.
Two recent series reporting the use of radiofrequency abla- tion for the treatment of adrenal tumors and ACC metastases indicated the feasibility, safety, and effectiveness of this proce- dure [17,18]. Wood et al. reported using RF for 16 primaries and metastatic adrenal tumors in eight patients [17]. In eight of 15 (53%) lesions a post-treatment loss of enhancement was observed and the lesions had stopped growing on follow-up CT scan after 6 months. Three of 16 lesions demonstrated inter- val growth, and four did not change in size. For smaller tumors with a maximum size less than or equal to 5 cm, eight of 12 tumors (67%) were completely ablated, as defined by decreas- ing size and complete loss of contrast enhancement. Three of 15 (20%) related RF lesions had nearly completely disappeared on imaging. Wood et al. considered RF to be effective for the short- term local control of small adrenal tumors and most effective for tumors less than 5 cm. These authors described a delayed multimicrobial abscesses in a 90-mm lesion 11 weeks after RF session, which was treated successfully with a long course of levofoxacin and prolonged catheter drainage. Mayo-Smith and Dupuy reported on the use of CT-guided percutaneous RF to treat 13 adrenal masses in 12 patients, 11 of which were metas- tases [18]. The results showed that 11 of 13 lesions were treated successfully with RF after one session. Only two large adrenal lesions (4 and 8 cm in size), associated with residual tumor after one treatment session, had to be treated repeatedly. No patient with metastases had recurrences at the treated site. One patient with thrombocytopenia that resulted from chemotherapy had a small hematoma, but no transfusion was required.
Regarding the potential benefits and disadvantages of PLA versus RF, it is our opinion that PLA has similar efficacy and complications as RF ablation with some advantages: more customizable geometries of the target lesions, smaller needle calibers, and MR imaging compatibility [19]. Most liver metas- tases in our patients were located adjacent or close (less than 1 cm away from) to vital structures such as vena cava (cases 3 and 4), body and tail of the pancreas and colon (case 1), beneath the capsule of the liver (cases 1 and 4). Nevertheless, using thin needles we were able to reach the tumors without difficulty with
much less risks of complications than the large bore needles with expandable prongs [20].
The combination with embolization using various chemotherapeutic agents can possibly improve the effi- cacy of percutaneous ablation techniques. Similar combined therapeutic strategies were described for the treatment of renal cell carcinomas [21] and hepatocellular carcinomas [22].
Although all other studies of percutaneous ablation in ACC did not address the issue of the clinical benefit, their findings and ours suggest that minimally invasive techniques can be a useful therapeutic option in patients for whom repeated surgical resection of tumors is not feasible. PLA induced an improvement of performance status, while the impact on survival of these techniques needs to be investigated in randomized trials. Until then, proper selection of patients who are candidates for these procedures will be critical in the assessment of their overall role in patient care.
Competing interests
The authors declare that they have no competing interests.
Acknowledgements
CMP and EP conceived the study and participated in data collection and analysis, RG participated in the data management; CMP, GB and SP carried out the percutaneous laser ablation procedure, RG and FMG participated in the data collection, RS analysed the data and prepared the manuscript.
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