Radiofrequency Ablation in Combination with Osteoplasty in the Treatment of Painful Metastatic Bone Disease

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1 Radiofrequency Ablation in Combination with Osteoplasty in the Treatment of Painful Metastatic Bone Disease Ralf Thorsten Hoffmann, MD, Tobias F. Jakobs, MD, Christoph Trumm, MD, Christof Weber, MD, Thomas K. Helmberger, MD, and Maximilian F. Reiser, MD PURPOSE: To evaluate the feasibility and effectiveness of combining radiofrequency (RF) ablation and osteoplasty for pain reduction in the treatment of painful osteolytic metastases. MATERIALS AND METHODS: Within 5 years, 22 patients (15 men and seven women; median age, 64 years) with 2 lesions located in the thoracic and lumbar spine, sacrum, pelvis, acetabulum, femur, and tibia were treated. Underlying tumors were breast, lung, renal cell, thyroid, cancer of unknown primary, and multiple myeloma. RF ablation was performed with the patient under moderate sedation and computed tomographic fluoroscopy guidance and was immediately followed by cement injection. Pain relief was evaluated with the visual analogue scale (VAS) score and the extent to which analgesics could be reduced. Clinical success was defined as a substantial reduction in pain and/o a reduced demand for analgesics, and technical success was defined as distribution of cement between both endplates of a vertebral body or at least 75% filling of osteolyses in other bones. RESULTS: Technical success and pain relief was achieved in all patients. Pain ratings with the VAS decreased from a mean of 8.5 to a mean of 5.5 after 24 hours P <.01), ( and a further decrease was detected after 3 months to P 3.5 < (.01). The amount or strength of analgesics was reduced in 15 patients and remained unchanged in five. In two patient the amount of analgesics increased due to tumor progression elsewhere. No major complication, no clinically obvious fracture of a formerly treated bone or treatment-related death, occurred. CONCLUSIONS: RF ablation and osteoplasty can be combined within one session and is both feasible and useful for the treatment of osteolytic bone metastases with regard to pain relief. J Vasc Interv Radiol 2008; 19: Abbreviations: PMMA polymethylmethacrylate, RF radiofrequency, VAS visual analogue scale DEPENDING on the underlying malignancy, painful osteolytic metastases frequently affected (1). In adults, skel- endings in the periosteum. Moreover, skull, and other long bones, are mostions affecting soft tissues and nerve can be detected in up to 70% of all etal metastases most often originate the mechanical stability of the affected patients during follow-up. Because from breast, lung, prostate, and renalbones is reduced, so that occult or frank metastatic spread predominates in cell cancer (1). More than 50% of allfractures of the affected vertebrae or those bones with a high proportion ofpatients develop severe pain during other bones develop. Standard therapies hematopoietic bone marrow, the their remaining lifetime 2) ( and have in those patients include surgery, che- radiation therapy, and the spine, followed by the pelvis, femur, pain caused by large bone destruc-motherapy, administration of analgesics (eg, morphine). Surgical treatments such as vertebrectomy, reconstructions with cages, tumor protheses, pedicle screws, From the Institute of Clinical Radiology, Ludwig- pondence to R.T.H.; rthoffma@med. Maximilians-University Campus Grosshadern, uni-muenchen.de Marchioninistr 15, Munich, Germany (R.T.H., T.F.J., C.T., M.F.R.); the Institute of Clinical and Diagnostic Radiology and Nuclear equally to this paper. Drs. RT Hoffmann and TF Jakobs contributed Medicine, Munich-Bogenhausen, Munich, Germany (T.K.H.); and the Institute of Diagnostic and None of the authors have identified a conflict of interest. Interventional Radiology, Klinikum-Deggendorf, Deggendorf, Germany (C.W.) Received June 28, SIR, ; final revision received September 4, 2007; accepted September 9, Address corres- DOI: /j.jvir or other types of extensive therapy 3) ( are associated with long recovery periods and high morbidity and mortality and should therefore be performed in patients with a longer life expectancy. Patients with a multifocal disease should undergo less-invasive, nonsurgical treatments to guarantee at least a 419

2 420 RF Ablation with Osteoplasty for Painful Bone Metastases March 2008 JVIR minimum of life quality for their remaining life span. In this situation, skeletal metastases may no longer be sensitive to chemotherapy, and additional radiation therapy may not be possible (eg, to avoid radiation-induced myelopathy). Moreover, side effects of analgesics may greatly reduce the quality of life (4). In this extremely difficult situation, the palliation of pain and prevention of imminent fractures are of utmost importance. Percutaneous vertebroplasty and osteoplasty are image-guided therapeutic procedures consisting in an injection of polymethylmethacrylate (PMMA) cement into a vertebral body or bone. They can be used in osteoporotic vertebral fractures (5 7) as well as in malignant lesions such as multiple myeloma and metastases (8,9). The principle of vertebroplasty has been extensively described in the medical literature (10 12) and includes pain reduction as well as stabilization and strengthening of the affected bone. Percutaneous radiofrequency (RF) ablation uses thermal energy for the destruction of the tumor and is widely accepted for the treatment of tumors or metastases within the liver (13,14), kidney (15), and even lung (16,17). Within the past few years, RF ablation has become a more and more accepted palliative therapy option in soft tissue tumors or bone destructions, and it allows for immediate pain relief (18 20). However, there are only few reports regarding a combination of RF ablation and osteoplasty in painful skeletal metastases (21 25). With RF ablation, necrosis of the tumor tissue can be achieved and, at the same time, pain relieved. Osteoplasty may also be used for pain relief and stabilization of bones affected by metastatic destructions. Therefore, the combination of therapies should have synergistic and complementary effects in these particular patients. The aim of this trial is the assessment of the efficacy, safety, and feasibility of a combination of these therapeutic options within a single treatment session. MATERIAL AND METHODS Patients At least 24 hours before undergoing the treatment, all patients or their legal Description of Patients Included in the Study and Their Underlying Diseases Pt. Number Gender Age Localization Primary 1 f 51 T 11 1 Breast Cancer 2 m 41 T 11, T 12, L 3 2 Renal cell carcinoma 3 m 49 T 2 CUP 4 m 72 L 5 Renal cell carcinoma 5 m 53 L 1 Renal cell carcinoma 6 f 64 L 5 & sacrum Multiple myeloma 7 f 67 L 5 Multiple myeloma 8 m 78 L 4 CUP 9 m 76 T 11 Multiple myeloma 10 f 47 S 1 3 Breast Cancer 11 m 61 L2&L3 Multiple myeloma 12 f 77 L 2 Breast Cancer 13 m 68 L 4 Lung cancer 14 m 72 T 8 & iliac bone Lung cancer 15 m 63 femur Multiple myeloma 16 m 72 iliac bone Thyroid cancer 17 m 49 acetabulum Thyroid cancer 18 m 81 tibia, acetabulum Renal cell carcinoma 19 f 62 femur CUP 20 m 86 acetabulum Renal cell carcinoma 21 f 64 sacrum Lung cancer 22 m 61 iliac bone Lung cancer 1 Thoracic spine number of vertebral body 2 Lumbar spine number of vertebral body 3 Sacrum number of vertebral body guardians gave written informed consent after receiving an explanation of the planned therapeutic intervention, alternative therapeutical options, and possible complications. All patients were treated according to the recommendations of the local tumor board. The approval of the local institutional review board was not necessary due to the character of the study as a retrospective analysis of formerly treated patients. Within a 5-year period ( ), 22 patients were treated with a combination of RF ablation and osteoplasty at our institution. The patient cohort was composed of 15 men and seven women aged years (median age, 64 years) at the time of the treatment. Patient characteristics are summarized in detail in the Table. Twenty-eight osteolyses were treated in these 22 patients. The lesions were located in the pelvis and acetabulum (n 6) (Fig 1), femur (n 2) (Fig 2), tibia (n 1), thoracic spine (n 6), lumbar spine (n 10) (Fig 3), and sacrum (n 2). The primary tumors were breast cancer (n 3), lung cancer (n 4), renal cell carcinoma (n 5), cancer of the thyroid (n 2), and osteolyses due to an underlying multiple myeloma (n 5). Furthermore, three patients had metastases from cancer of unknown primary (CUP). In three cases, the origin of the primary tumor was unknown. All patients were treated with various analgesics and had a history of various chemotherapeutic regimens. RF Ablation All treatments were performed with the patient under moderate sedation with midazolam (Dormicum; Roche- Pharma, Grenzach, Germany) and piritramide (Dipidolor, Janssen-Cilag, Neuss, Germany) together with local anesthesia (Scandicain; Astra-Zeneca, Wedel, Germany). Pulse and oxygen saturation were measured in all patients by using pulse oximetry. Oxygen was given on demand via a face mask. Depending on the location of the tumor, patients were positioned on the computed tomographic (CT) table in a prone, oblique, or supine position. In all patients, the RF electrode was positioned under CT fluoroscopy by using a single-section, four-section, or 16-section multidetector CT unit (Somatom Plus 4, Sensation 4, and Sensation 16, respectively; Siemens Medical Solutions, Forchheim, Germany) by

3 Volume 19 Number 3 Hoffmann et al 421 Figure 1. (a, b) Images in a man (patient no. 17) with a painful metastasis of an underlying renal cell carcinoma with substantial destruction of the pelvic bone (arrow). (c) RF ablation was performed by using a multitined expandable RF electrode with a diameter of 3 cm. (d) Immediately after RF ablation, cement (arrow) was injected with a pressure syringe. (e) The therapy was successful in terms of pain relief. The cement distribution was sufficient (arrow). No substantial leakage is demonstrated. using the hand-care mode to reduce radiation exposure to the interventionalist and the patient. Fifteen patients were treated with the monopolar RITA Starburst XL elecrode (RITA Medical Systems, Mountain View, Calif) with nine deployable electrodes (maximum peripheral diameter of the extended electrodes, 5 cm), which enabled the treatment of lesions of 2 5 cm in diameter. In seven patients, a monopolar, multitined expandable LeVeen electrode (Radiotherapeutics; Boston Scientific, Natick, Mass) was used, with the diameter of the expandable electrode adapted to the size of the tumor (3 5 cm). The access path was created by using a bone biopsy cannula (Somatex Spicut; Teltow, Germany) under CT fluoroscopic guidance with the use of a small surgical hammer because this technique for inserting the cannula provides very good control with regard to an exact needle placement. After the access was created, the biopsy cannula was removed and the RF electrode inserted. The ablation protocols were adapted to those provided by the manufacturer of the RF generators. Because the aim of the RF ablation was to destroy as much of the tumor tissue as possible, electrodes were either fully deployed or a composite ablation technique was applied. Depending on the generator used, completion of the ablation procedure was defined either by reaching the target temperature (95 C in average of the five thermocouples within the array) and holding it for at least 15 minutes or by reaching the so-called roll-off (ie, the substantial increase of impedance resulting in the loss of alternating current flow) twice, indicating complete coagulation necrosis. The time to achieve the target temperature or the first roll-off differed among the patients depending on the location of the tumor and the proximity of the tines to vessels causing the perfusion-mediated tissue cooling. When the treatment was completed, the electrode array was retracted and a track ablation performed during withdrawal of the electrode to avoid tumor cell seeding along the needle tract and to prevent bleeding with coagulation of small vessels. Vertebroplasty and Osteoplasty Immediately after completion of the RF ablation, the RF probe was replaced with a 10- or 15-gauge vertebroplasty cannula (CementoRe set; Optimed, Ettlingen, Germany) under CT fluoroscopic guidance, and PMMA bone cement (Bone Cement V; Biomed, Ride, Switzerland) was prepared. Osteoplasty and vertebroplasty were performed by using a 10-mL pressure syringe (CementoRe set) under CT fluoroscopic guidance. Vertebroplasty and osteoplasty were determined to be complete and, therefore, technically successful if

4 422 RF Ablation with Osteoplasty for Painful Bone Metastases March 2008 JVIR Figure 2. (a) Osteolysis of a metastasis within the femur caused by a renal cell carcinoma. The patient (no. 18) had substantial pain. (b) An access path was created by using a bone biopsy cannula, and the RF electrode was inserted and fully deployed with the patient under moderate sedation. (c) After RF ablation, a vertebroplasty cannula was inserted and PMMA administered. (d) Control scan obtained 24 hours later shows a good distribution of the cement. The osteolysis is almost completely filled. the cement was detectable between both endplates of a vertebra or filled more than 75% of the osteolysis in other bones, respectively. After the needle was withdrawn, all patients underwent a control CT examination (volume helical scan with three-dimensional reconstruction) and were observed for at least 24 hours in a ward. This was followed by another CT examination that served as the first baseline study and helped detect potential early adverse events. Follow-up After discharge, the patients entered a follow-up program where we kept in close contact with the patients and their referring physicians to obtain information about late adverse events. All patients were asked before treatment and at follow-up interviews to answer a standardized questionnaire. The questionnaire included a visual analogue scale (VAS) with questions about analgesics and subjective well-being. The VAS was assigned a rating from 0 to 10, with 0 indicating no pain and 10 indicating the worst pain. Clinical success was defined as a significant reduction of pain as demonstrated with the VAS score and/or a significant reduction in the amount of analgesics needed by the patient. The VAS scores were analyzed with a paired t test. A P value of less than.05 was considered indicative of a statistically significant difference. The patient s subjective estimation about their situation, the assessment

5 Volume 19 Number 3 Hoffmann et al 423 Figure 3. (a) Image in patient no. 13 with an osteolytic metastasis of a bronchial carcinoma. (b) Sagittal reconstruction of the CT scan obtained before treatment. Surgical stabilization was already performed (arrow). However, the patient had unbearable pain due to the large osteolysis. (c) RF ablation was performed with the patient under moderate sedation. Because of the large size of the tumor, a composite ablation was performed after the electrode was repositioned. (d) Percutaneous vertebroplasty was performed under CT fluoroscopy immediately after thermal ablation. (e) Control scan obtained 24 hours later shows a very good result, with PMMA between both endplates (arrow). The patient also had substantial pain relief. of the complication rate (including clinically obvious fractures of the treated area), and the change in analgesics were also subjects of analysis. RESULTS In all patients, RF ablation was possible in terms of complete ablation of the targeted tumor volume. The subsequent vertebro- and osteoplasties, respectively, were also successful in all patients in terms of filling of the targeted lesion. In all patients, moderate sedation was sufficient and no single treatment had to be aborted due to pain or incompliance of the patients. No major complication occurred in this patient collective. In eight of the 14 patients with metastases of vertebral bodies, a small amount of cement leakages into the paravertebral soft tissue and toward the spinal canal was detected in six and two patients, respectively. All cement leakages remained without clinical consequences for the patients. In two patients, a hematoma at the insertion point of the needle occurred, also without any clinical consequences. The 28 lesions were treated with 36 RF sessions (1.3 sessions per lesion and 1.7 sessions per patient). The amount of PMMA used was ml (mean, 2.9 ml) for lesions within the vertebral body; ml (mean, 8.7 ml) for bone destructions within the sacrum, acetabulum, and pelvis; and ml (mean, 6.7 ml) for lesions within the long bones. Pain relief was achieved within 24 hours in all patients. Two patients complained of pain for at least 3 days within the soft tissue crossed by the RF probe; however, no further treatment was necessary. Pain ratings with the VAS decreased from a mean of 8.5 to a mean of 5.5 after 24 hours (P.01), and another decrease was detected after 3 months to 3.5 (P.01). In six patients, pain recurred during follow-up because the malignant disease recurred within other parts of the body. In five of these patients, another osteoplasty in combination with RF ablation in a vertebral body was performed; one patient had a new osteolysis within the pelvis. During a mean follow-up of 7.7 months (range, 3 15 months), 15 patients were able to reduce the amount of analgesics or were able to take weaker analgesics (nonopioids instead of opioids). In five patients, the analgesics remained unchanged. Two patients had to take more or stronger medication because of rapid tumor progression elsewhere. DISCUSSION Depending on the underlying metastatic disease, osteolytic metastases occur in up to 70% of patients (1), and more than 50% of those patients develop intractable pain during the course of their disease (2). Surgery, chemotherapy, and analgesics, as well as radiation therapy, are the standard treatments in patients with bone destructions due to skeletal metastases. With radiation therapy, partial or complete pain relief can be achieved within days after the beginning of the radiation therapy, and the maximum benefit is obtained after weeks (21). The late onset of pain alle-

6 424 RF Ablation with Osteoplasty for Painful Bone Metastases March 2008 JVIR viation after radiation therapy especially in patients with unbearable pain is not acceptable. Therefore, vertebroplasty plays an invaluable role in the treatment of osteolytic, painful vertebral bodies, reducing the risk of vertebral fracture and the grade of pain. With vertebroplasty, pain palliation can be achieved in 50% 97% of patients (26 29). It is interesting that Cotton et al (27) described partial or complete pain relief in 36 of 37 patients within 6 72 hours of PMMA injection, independent from the percentage of cement filling in the vertebral body. Weill et al (30) found, in patients who had an immediate significant benefit, no recurrence of pain at 1-month follow-up. Seventy-five percent of those patients still had no pain 3 months after therapy (30). The remaining 25% of patients with recurring pain were determined to have new metastases adjacent to the formerly treated area, a finding that suggested that the recurring pain is due to tumor relapse instead of a failure of the initial procedure. The mechanism for this significant pain reduction as described in many scientific articles is presumably based on the stabilization of invisible microfractures. Moreover, during hardening of the PMMA there is a significant thermal effect that results in damage to adjacent sensible nerves and the destruction of tumor tissue (31). Various authors described osteoplasty in the treatment of osteolyses of the pelvis, sacrum, and femur and were able to show that this therapeutic approach is effective in up to 92% of patients after hours (8,24,30). Thermal ablative therapies play an important role in the treatment of painful metastases involving the bone (18,32). RF ablation is the most common form of thermal ablative therapy within the liver and beyond, and most of the articles about bone and soft tissue treatments deal with its use. Cryoablation and laser-induced tumor therapy, however, are used by only a few groups (33,34). Until now, there have been only case reports or small series of patients treated with RF ablation for pain caused by metastatic bone destructions or soft tissue tumors involving bone. All studies and reports, however, showed that RF ablation is effective and allows for immediate pain relief (18,35). Goetz et al (20) published their results of a multicenter trial that included 62 patients, and a success rate regarding pain relief of nearly 80% was reported. The authors were able to show the importance of covering the tumor-bone interface completely to achieve sufficient pain relief, whereas debulking of large tumors with no adequate coverage of the tumor-bone interface had no significant effect on the complaints of the patients. Various factors may contribute to the therapeutic effect of RF ablation, such as the reduction of interleukins and TNF responsible for a sensitization of nerve endings and the inhibition of osteoclasts. The most important mechanism for the immediate pain alleviation may be the destruction of sensible nerve endings within the periosteum (36,37). The conclusion of that multicenter trial was that RF ablation is a powerful method for treating pain, with an immediate response in otherwise untreatable patients. There are only few reports about the combination of RF ablation and vertebroplasty, and there are even fewer reports about the combination of both therapies in a single session (21 23). In addition to the pain-reducing effect of each therapy alone, the use of ablation before osteoplasty destroys tumor tissue and therefore makes osteoplasty safer because tumor vessels are obliterated and the consistency of the tumor is changed, so that bone cement can more easily distribute within the lesion. The effect of altering the consistency of the tumor by applying heat similar to the effect of cooking meat can shrink the tumor and destroy the cohesion of the tumor cells. This effect may be responsible for a more homogeneous distribution of the cement during osteoplasty compared with the results the authors achieved in patients treated with vertebroplasty alone. To the best of our knowledge, however, there are no studies available that deal with that topic. In our study, pain relief was achieved in all patients (100%), which is slightly better than the effect (50% 97%) described after vertebroplasty by other authors (26,28). About 70% of the patients (15 of 22) were able to reduce the dose of their analgesics, which is comparable to the results described by Goetz et al (20) after RF ablation. The two-step reduction of the VAS rating after 24 hours to a minimum after 3 months might be due to the relief of pain caused by passing the soft tissues with the bone biopsy cannula, RF electrodes, and vertebroplasty needles as well as to the track ablation. Taking the palliative situation of the patients into account, the long-lasting effect of the combined therapy with no more pain at the area treated in our study, together with the low rate of complications and the possibility to perform this combined procedure during a single session and with a short stay in the hospital, makes this therapy an attractive option. There indeed are some limitations of this study. First, it is a retrospective analysis of the outcome of formerly treated patients. Therefore, no control group exists showing the superiority of a combination of both therapies over each single treatment alone. Another limitation is the inhomogeneous patient group. The patients included in our study had different underlying tumor types, and the osteolyses treated were in different locations. However, all patients had osteolytic metastases that caused unbearable pain and did not respond to conventional therapies. Another possible drawback of our study is the missing radiologic follow-up to especially show changes in vertebral height after treatment. Therefore, we are only able to state that there were no clinically obvious fractures in the formerly treated areas at follow-up. From our retrospective study, we can conclude that RF ablation and vertebro- and/or osteoplasty are minimally invasive methods that can be used alone or in combination to treat patients with otherwise untreatable pain due to metastatic destructions within the bone. RF alone can reduce pain almost immediately; however, it is not able to strengthen the bone weakened by neoplastic infiltration. Osteoplasty, however, stabilizes microfractures occurring within the destroyed bone, strengthens the bone, and adds an additional effect due to the heat occurring during hardening of the PMMA. The combination of both therapies may have a synergistic effect. Immediate pain relief is presumably caused by RF ablation of sensible nerve endings, a longer-lasting effect occurs due to tumor destruction

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