European Journal of Radiology
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1 European Journal of Radiology 77 (2011) Contents lists available at ScienceDirect European Journal of Radiology journal homepage: Percutaneous treatment of bone tumors by radiofrequency thermal ablation Fernando Ruiz Santiago a,, María del Mar Castellano García a, Luis Guzmán Álvarez a, Jose Luis Martínez Montes b, Manuel Ruiz García a, Juan MIguel Tristán Fernández a a Department of Radiology, Hospital of Traumatology (Ciudad Sanitaria Virgen de las Nieves), Carretera de Jaen SN, Granada, Spain b Department of Traumatology, Hospital of Traumatology (Ciudad Sanitaria Virgen de las Nieves), Carretera de Jaen SN, Granada, Spain article info abstract Article history: Received 29 September 2008 Received in revised form 5 May 2009 Accepted 9 June 2009 Keywords: Bone neoplasm therapy Palliation Ablation We present our experience of the treatment of bone tumors with radiofrequency thermal ablation (RFTA). Over the past 4 years, we have treated 26 cases (22 benign and 4 malignant) using CT-guided RFTA. RFTA was the sole treatment in 19 cases and was combined with percutaneous cementation during the same session in the remaining seven cases. Our approach to the tumors was simplified, using a single point of entrance for both RFTA and percutaneous osteoplasty. In the benign cases, clinical success was defined as resolution of pain within 1 month of the procedure and no recurrence during the follow-up period. It was achieved in 19 out of the 21 patients in which curative treatment was attempted. The two non-resolved cases were a patient with osteoid osteoma who developed a symptomatic bone infarct after a symptom-free period of 2 months and another with femoral diaphysis osteoblastoma who suffered a pathological fracture after 8 months without symptoms. The procedure was considered clinically successful in the five cases (4 malign and 1 benign) in which palliative treatment was attempted, because there was a mean (±SD) reduction in visual analogue scale (VAS) pain score from 9.0 ± 0.4 before the procedure to <4 during the follow-up period Elsevier Ireland Ltd. All rights reserved. 1. Introduction Image-guided radiofrequency thermal ablation (RFTA) is a branch of interventional oncology that uses direct application of radiofrequency-generated heat to coagulate and destroy tumor tissue [1]. It has been applied to treat benign bone tumors and tumor-like lesions as a single modality or as an adjunct to surgical therapy [2]. It has proven useful in metastatic disease as a palliative measure to relieve disabling pain [3]. Percutaneous delivery of polymethylmethacrylate has been used to relieve pain in patients with vertebral and skeletal neoplasms and prevent pathological fractures. The injection of bone cement into the lesion reduces the pain and stabilizes the bone [4,5]. A combination of these two procedures is useful to achieve both destruction of tumor tissues and strengthening of bone architecture. We present our experience with the percutaneous treatment of bone lesions by RFTA and/or cementoplasty under CT guidance. We discuss the indications for RFTA combined with cementoplasty Corresponding author at: C-Julio Verne 8, 7B, Granada, Spain. addresses: ferusan@ono.com, ferruizsan@terra.es (F. Ruiz Santiago). and the usefulness of RTFA alone, especially for intra-articular tumors. 2. Patients and methods Twenty-six patients (13 males) were treated with CT-guided RFTA at our center from 2003 to The history of symptoms before RFTA treatment ranged from 3 to 28 months (mean of 18 months). General anesthesia was used in 15 cases, epidural in 6, and local nerve blockage in 4. RFTA was applied as a single modality in 19 patients and was combined with percutaneous cementation in 7 patients. Table 1 summarizes the characteristics of patients and their treatments. A simplified approach to the tumors was adopted, using a single entry point for both the RFTA and percutaneous osteoplasty. A hammer, vertebroplasty needle (100 cm, 13 or 10 G), and biopsy trephine (150 cm, 13 or 15 G) were used to reach the bone lesions and create an entry channel for the electrode (Fig. 1). The whole bone tumor was imaged for selection of the optimal route to achieve its complete treatment with the minimum number of ablations. An intramuscular needle introduced into the selected entry point guides the thicker vertebroplasty needle into the bone, monitoring its progress on CT. In the vicinity of sensitive anatomic X/$ see front matter 2009 Elsevier Ireland Ltd. All rights reserved. doi: /j.ejrad
2 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) Table 1 Summary of treated cases. N: number of cases (intra-articular cases). Diagnosis N Cementation Age Tumor size (cm) Number of sessions Technical success Clinical success Osteoid osteoma 14 (4) ± ± ± Osteoblastoma ± ± Chondroblastoma 2 (1) ± ± Hemangioma Enchondroma Eosinophilic Granuloma Giant cell tumor 1 (1) Metastasis 3 (3) ± ± ± Myeloma (9) Values are expressed as mean ± standard error of the mean. Fig. 1. Basic tools. placement of the electrode, the cannula was withdrawn without displacing the electrode to avoid contact between metal needle and active electrode tip, which could burn the needle pathway or skin. After checking the correct position of the electrode by CT, a dry ablation was performed for 6 min. In large lesions, this process was repeated from a different entry point. Cementation was indicated in tumors arising in weight-bearing bones and when a risk of pathological fracture was suspected. In these cases, we placed the cannula into the appropriate intra-tumor site immediately after the ablation(s), using the radiofrequency electrode as guide. It was frequently necessary to fit a stylet within the cannula to correct the tip position. The lesion was then filled with the appropriate amount of cement, monitoring the process by fluoroscopy using a mobile C-arm unit. A rapid CT scan was performed during the procedure in some cases (Fig. 4). A Radionics radiofrequency generator (Tyco Healthcare Group, Burlington, MA, USA) was used; generator output was W and display parameters were impedance, ; current, ma; power, W; and temperature, 0 99 C. Power was increased manually until the desired temperature was attained. Radionics Cool-tip monopolar electrodes were used: 17-G (4.5 Fr), length cm and exposure tip 1 3 cm. structures (blood vessels, nerves), damage was avoided by introducing the needle in short, careful steps (Fig. 2). When the needle reached the edge of the tumor (Fig. 3), a biopsy trephine was coaxially introduced to obtain material for the pathology study and to serve as a channel for the radiofrequency electrode. After correct Fig. 2. Entry of vertebroplasty needle close to sciatic nerve (arrow). Previous introduction of an intramuscular needle helps to select the appropriate path for the thicker trephine. Fig. 3. (A) Intra-articular osteoid osteoma. (B) Introductory cannula at the edge of the nidus. (C) Biopsy trephine within the nidus. (D) Electrode inside the nidus with the cannula withdrawn.
3 158 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) Fig. 4. Chondroblastoma of the femoral head during ablation and cementation procedures. X-rays are shown before and after treatment. CT and MR studies were performed in all patients. CT images were acquired with a multi-detector row CT scanner (HiSpeed Advantage Qx/I; GE Medical Systems, Milwaukee, WI). MR images were obtained using a 1.5-T MR scanner (Signa Horizon; GE Medical Systems). Technical success was recorded if the tumor was treated according to protocol and was completely ablated [1,6]. Clinical success was evaluated according to a visual analogue scale (VAS) score (range, 0 10). Patients were asked to rate their average pain (0 = no pain, 10 = pain as bad as can be imagined). Mean VAS scores before treatment and at 1 month, 6 months, and 1 year after therapy were compared. Two groups were considered for the statistical analysis: a curative treatment group, including patients with benign lesions in which complete destruction of the tumor was attempted (n = 21); and a palliative treatment group, including the four patients with malignant tumors and one with benign unresectable sacral giant cell tumor (n = 5). In the curative treatment group, clinical success was defined as resolution of pain within 1 month of the procedure and no recurrence within the follow-up period. In the palliative group, success was defined by a statistically significant reduction in pain and by the patient s evaluation that it was a worthwhile procedure. Pain response was statistically analyzed by using the Student s t-test for related samples. 3. Results In the curative treatment group, the VAS score decreased from 8.0 ± 0.2 before treatment to mean values <1 during the follow-up period (Table 2). Technical success was achieved in 20 out the 21 patients in this group. The unsuccessful case was an eosinophilic granuloma localized in the iliac wing. In this patient, the vertebroplasty needle broke on the edge of the bone during the pre-ablation withdrawal and was maintained in place while three ablation sessions were performed at different depths (Fig. 5). The pain resolved and there was no increase in lesion size and no activity (by scintigraphy) 1 year later. A subsequent CT showed the lesion to be sclerotic. Out of the 21 patients with benign lesion, 19 reported complete pain relief during the follow-up period. Clinical failure was recorded in 1 case of tibial osteoid osteoma and 1 case of femoral osteoblastoma. The patient with the tibial osteoid osteoma suffered a painful bone infarction (Fig. 6) after a 2-month symptom-free period. Surgical removal of necrotic bone tissue was performed elsewhere, achieving initial disappearance of symptoms; at 6 months later, the patient still reports sporadic pain that requires analgesia. No further surgical therapy has been recommended. The femoral osteoblastoma was asymptomatic during 8 months after the procedure until the patient suffered a pathological fracture when twisting her leg after catching it in a cable on the floor. Intramedullary nailing was performed (Fig. 7). In the palliative treatment group, the VAS decreased from a mean value of 9.0 ± 0.4 to mean values <4 (Table 2). Technical success was not possible in any of these five cases because ablation of the whole tumor was impeded by the presence of sensitive anatomic structures (vessels and nerves) within or adjacent to Table 2 Comparison of VAS scores before ablation and at 1-month, 6-month and 1-year follow-ups). Type of treatment Visual analogue scale (VAS) Significance (P) Before 1 month 6 months 1 year Curative (21) 8.0 ± ± ± ± 0.1 <0.001 Palliative (5) 9.0 ± ± ± ± 0.3 <0.01
4 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) Fig. 5. Cannula needle was broken during withdrawal (A). The broken fragment was left inside iliac bone (B). Fig. 6. Osteoid osteoma of the outer cortex of the tibia. After the procedure, the patient developed a symptomatic bone infarct shown in this coronal DP fat-sat MR imaging (TR: 1900, TE: 44). tumor tissues. Nevertheless, the pain improvement was sufficient for the procedure to be considered worthwhile by all patients. 4. Discussion Image-guided RFTA reduces pain, improving function and quality of life in patients with painful bone tumors. It has been used to treat benign bone tumors and tumor-like lesions as a single modality or as an adjunct to surgical therapy. RFTA also offers an alternative method for the palliation of localized painful osteolytic metastatic lesions [7]. CT-guided radiofrequency has become the standard treatment of most osteoid osteomas [2]. However, indications for RFTA treatment are expanding to include other benign bone conditions such as giant cell tumor, chondroblastoma, osteoblastoma, hemangioma, eosinophilic granuloma, and enchondroma [8,9]. RFTA is only indicated in osteoid osteomas when a presumptive diagnosis is made based on history, clinical examination, and imaging. TC 99 scintigraphy still plays an important role in defining an active lesion as an area of increased uptake. In 1992, Rosenthal was the first to report technical and clinical success with RFTA in osteoid osteomas [10]. The intra-articular localization of osteoid osteomas implies an additional challenge for percutaneous treatment and has been related to a greater probability of recurrence [11]. The hip is the most commonly involved joint. Although an extra-articular approach has been advocated [12] to minimize the risk of septic joint infection or avoid articular cartilage damage, we preferred the most direct route to the lesion, even when it passed through the joint or a non-weight-bearing area of the cartilage (Fig. 3). The small gauge (13 G) of the needle used led to minimal damage of articular structures. An extra-articular approach is technically more complex. For example, in the hip, it would require a bone channel through trochanter and femoral neck, as in orthopedic surgery, resulting in a longer and more aggressive procedure [13]. Most series reporting on the radiofrequency ablation of osteoid osteoma have described a clinical success rate of %, with few complications and a short length of hospital stay [2,14,15]. This is in agreement with our experience, since only 1 out of 14 cases did not respond to initial treatment (7%), due to development of a symptomatic bone infarct. Chondroblastomas are benign cartilaginous lesions that usually affect patients under 20 years old. They are frequently found at the epiphysis or apophysis of an immature skeleton, hampering their surgical removal. RFTA has been proposed as an alternative approach for the curative therapy of these tumors [8]. Ablation was followed by percutaneous cementation in the two cases (hip and knee) in the present study. The aim in the hip case was to avoid depression of the cortical bone in a weight-bearing area, and the patient remains asymptomatic after 4 years. In the knee case, a small amount of cement was introduced to reinforce the thermal effect of the RFTA with the exothermic effect of the cement and to strengthen the bone. The patient remains asymptomatic after 1 year.
5 160 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) Fig. 7. Osteoblastoma of the anterior femoral cortex. Images show the lesion before the procedure (A and C), during ablation (B) and the pathological fracture suffered 8 months later (D). Osteoblastoma is a rare, benign, bone-forming tumor that is histologically related to the more common osteoid osteoma. It is also a tumor of younger individuals, with almost 90% of patients being diagnosed before 30 years of age. Despite its benign nature, the tumor may exhibit aggressive behavior and become larger than an osteoid osteoma ( 2 cm). Recurrences are not uncommon after classical treatment by surgical excision or curettage [16]. RFTA is a less invasive alternative. It is performed in the same way as in osteoid osteoma, using electrodes with a long active tip or a larger number of ablation sessions [17]. There have been fewer reports on the treatment of other benign bone conditions such as giant cell tumor, enchondroma, eosinophilic granuloma, or bone hemangioma. However, the treatment outcomes in the patients with these diagnoses in the present series were considered good in relation to pain control and the arrest of growth in follow-up studies. Our review of the literature only found reports on the treatment of bone chondroma [9], eosinophilic granuloma [18], and bone hemangioendothelioma [19]. RFTA has also been used as an alternative therapy or as a complement to the irradiation and surgical treatment of metastatic bone lesions of the spine, pelvis, and long bones [3,7]. The main goals of percutaneous CT-guided radiofrequency ablation of bone metastases are pain relief and local control of tumor growth. Several studies have reported satisfactory results, with a reduction in pain and a preservation or improvement of neurological function without major complications [7,20]. Our experience with metastatic disease is limited to 4 patients, but good pain control outcomes were obtained in all cases. One patient with acetabular thyroid metastasis and another with sacral metastasis required a further session of ablation at 4 and 6 months, respectively, after the first procedure. A combination of radiofrequency ablation and percutaneous cementoplasty using polymethylmethacrylate may be important to stabilize impending fractures due to metastatic disease. This procedure has yielded excellent stabilization and pain relief with a subsequent improvement in quality of life without major complications in the treatment of osteolytic tibial plateau [21] and talus metastases [3]. The clinical utility of this combined therapy has been reported in several studies, but experience with this technique remains limited [21,22]. The combined use of RF ablation and cementoplasty appears to be useful in achieving tumor necrosis and stabilizing the ablated lesions. The coagulation necrosis produced by RF ablation may promote a homogenous distribution of the bone cement within the ablated lesion [21]. We used cementation in combination with RFTA in the four malignant cases, the sacral giant cell tumor and two chondroblastomas in order to support weakened bone at the ablated sites
6 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) Fig. 8. Axial MR post-contrast T1 weighted imaging (TR: 800, TE: 11) (B) and CT (B) of a lytic lesion of sacrum and iliac bone secondary to hypernefroma. After ablation (C), cementation is performed close to normal bone (D). (Fig. 8). Careful fluoroscopy monitoring allowed us to detect any leakage. Although a high cement filling percentage was achieved in the chondroblastomas (Fig. 4), we did not attempt to fill the whole tumor in the remaining cases. These lesions expanded and deformed the normal bone and there was high risk of damage to vascular or neural structures trapped by the tumor. It has been reported that smaller volumes are usually adequate in tumor disease, when the aim of cement injection is pain relief [23]. We selected sites close to interfaces with normal bone in order to avoid progression toward healthy bone structures. We also believe that bone cement may be useful as a marker of ablated areas for any future ablation sessions that might prove necessary. Complete ablation of larger tumors is not mandatory, since treatment at the interface between tumor and periosteum is sufficient to provide symptomatic relief [24]. Possible complications of RFTA and percutaneous cementation have been described elsewhere [25,26]. In the present study, adverse events after the procedure were noted in 4/26 (15%) patients. Although necrosis after RFTA usually remains asymptomatic, one patient with tibial osteoid osteoma developed a symptomatic bone infarct (Fig. 6). We speculate that the necrotic tibial tissue might have produced a mechanical overload that made reactive bone tissue symptomatic. Pain was absent for 6 months after removal of the necrotic tissue but then returned, probably due to the same mechanical problem. One patient with acetabular thyroid metastases developed protrusio acetabuli (Fig. 9). In weight-bearing joints and lesions near the articular cartilage, there is a risk of cartilage damage and mechanical weakening of the bone due to lack of bone replacement in ablated areas [8]. This acetabular fracture would have likely occurred without RFTA, and we do not know whether this treatment shortened or lengthened the time to fracture. One case of femoral diaphysis osteoblastoma developed a pathological fracture 8 months after the treatment (Fig. 7). Although some fractures have been described shortly after RFTA [7], it is not known whether the fractures were due to the treatment or to the underlying bone disease. We may have underestimated the risk of pathological fracture in our patient. According to Mirels s scoring system for metastatic bone disease, a tumor presenting a maximum destruction (1/3 to 2/3 of bone) in any radiographic view has a moderate risk of pathological fracture [27]. Therefore, intramedullary cementation during the same procedure may have avoided the subsequent pathological fracture in the present case. The vertebroplasty needle broke during treatment of eosinophilic granuloma of the iliac wing (Fig. 5), a possible complication of any orthopedic procedure. It probably occurred because of the decision to approach the lesion through the iliac bone, and another pathway may have been more appropriate. If it is necessary to pass through hard bone pathway, it is advisable to use a bone trochar or drill to facilitate the entry of the needle.
7 162 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) Fig. 9. Thyroid acetabular metastasis. Axial T2 weighted (TR: 4160, TE: 97) (A) and coronal T1 (C) weighted MR imaging before treatment and CT during ablation (B). Protrusio acetabuli developed within 5 months post-procedure, as shown in the coronal T1 weighted images (TR: 460, TE: 11.58) (D). In summary, percutaneous RFTA and cementation can be curative in small benign bone tumors and palliative in larger lesions or malignant bone tumors. We present a technique that uses a single approach for both RFTA and cementation. References [1] Goldberg SN, Grassi CJ, Cardella JF, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria. Radiology 2005;235: [2] Rosenthal DI, Hornicek FJ, Torriani M, Gebhardt MC, Mankin HJ. Osteoid osteoma: percutaneous treatment with radiofrequency energy. Radiology 2003;229: [3] Callstrom MR, Charboneau JW, Goetz MP, et al. Painful metastases involving bone: feasibility of percutaneous CT- and US-guided radio-frequency ablation. Radiology 2002;224: [4] Hierholzer J, Anselmetti G, Fuchs H, et al. Percutaneous osteoplasty as a treatment for painful malignant bone lesions of the pelvis and femur. J Vasc Interv Radiol 2003;14: [5] Kallmes DF, Jensen ME. Percutaneous vertebroplasty. Radiology 2003;229: [6] Goldberg SN, Grassi CJ, Cardella JF, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria. J Vasc Interv Radiol 2005;16: [7] Callstrom MR, Charboneau JW, Goetz MP, et al. Image-guided ablation of painful metastatic bone tumors: a new and effective approach to a difficult problem. Skeletal Radiol 2006;35:1 15. [8] Tins B, Cassar-Pullicino V, McCall I, et al. Radiofrequency ablation of chondroblastoma using a multi-tined expandable electrode system: initial results. Eur Radiol 2006;14(6): [9] Ramnath RR, Rosenthal DI, Cates J, et al. Intracortical chondroma simulating osteoid osteoma treated by radiofrequency. Skeletal Radiol 2002;31: [10] Rosenthal DI, Alexander A, Rosenberg AE, Springfield D. Ablation of osteoid osteomas with a percutaneously placed electrode: a new procedure. Radiology 1992;183: [11] Cribb GL, Goude WH, Cool P. Percutaneous radiofrequency thermocoagulation of osteoid osteomas: factors affecting therapeutic outcome. Skeletal Radiol 2005;34: [12] Pinto CH, Taminiau AHM, Vanderschueren GM, et al. Technical considerations in CT-guided radiofrequency thermal ablation of osteoid osteoma: tricks of the trade. AJR 2002;179: [13] Sticker SJ. Extraarticular endoscopic excision of femoral head chondroblastoma. J Ped Orthop 1995;15: [14] Lindner NJ, Ozaki T, Roedl R, et al. Percutaneous radiofrequency ablation in osteoid osteoma. J Bone Joint Surg Br 2001;83: [15] Torriani M, Rosenthal DI. Percutaneous radiofrequency treatment of osteoid osteomas. Pediatr Radiol 2002;32: [16] Frassica FJ, Waltrip RL, Sponseller PD, et al. Clinicopathologic features and treatment of osteoid osteoma and osteoblastoma in children and adolescents. Orthop Clin North Am 1996;27: [17] DiCaprio MR, Bellapianta JM. Use of radiofrequency ablation in the treatment of bone tumors. Techn Orthop 2007;22(2): [18] Corby RR, Stacy GS, Peabody TD, et al. Radiofrequency ablation of solitary eosinophilic granuloma of bone. AJR 2008;190: [19] Rosenthal DI, Treat ME, Mankin HJ, et al. Treatment of epithelioid hemangioendothelioma of bone using a novel combined approach. Skeletal Radiol 2001;30: [20] Gronemeyer DH, Schirp S, Gevargez A. Image-guided radiofrequency ablation of spinal tumors: preliminary experience with an expandable array electrode. Cancer J 2002;8:33 9. [21] Schaefer O, Lohrmann C, Herling M, et al. Combined radiofrequency thermal ablation and percutaneous cementoplasty treatment of a pathologic fracture. J Vasc Interv Radiol 2002;13: [22] Schaefer O, Lohrmann C, Markmiller M, et al. Combined treatment of a spinal metastasis with radiofrequency heat ablation and vertebroplasty. AJR 2003;180: [23] Gangi A, Wong LLS, Guth S, et al. Percutaneous vertebroplasty: indications, techniques and results. Semin Intervent Radiol 2002;19: [24] Kojima H, Tanigawa N, Kariya S, et al. Clinical assessment of percutaneous radiofrequency ablation for painful metastatic bone tumors. Cardiovasc Intervent Radiol 2006;29:
8 F. Ruiz Santiago et al. / European Journal of Radiology 77 (2011) [25] Goetz MP, Callstrom MR, Charboneau JW, et al. Percutaneous image-guided radiofrequency ablation of painful metastases involving bone: a multicenter study. J Clin Oncol 2004;22(2): [26] Nussbaum DA, Gailloud P, Murphy K. A review of complications associated with vertebroplasty and kyphoplasty as reported to the food and drug administration medical device related web site. J Vasc Interv Radiol 2004;15: [27] Mirels H. Metastatic disease in long bones. A proposed scoring system for diagnosing impending pathologic fractures. Clin Orthop Relat Res 1989;249:
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