Cryotherapy Of Musculoskeletal Tumors From Basic Science To Clinical Results
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1 Technology in Cancer Research & Treatment ISSN Volume 3, Number 4, August (2004) Adenine Press (2004) Cryotherapy Of Musculoskeletal Tumors From Basic Science To Clinical Results Combined modality treatment of musculoskeletal tumors led to improved patient survival. As survival improves, more consideration is given to the functional outcome of treatment, and interest is focused on the development of less mutilating and extensive surgery. One modality that can reduce patient disability significantly is cryosurgery, as it allows minimally invasive surgery based on marginal resection and tumor interface sterilization instead of wide resection of certain neoplasms. Classical cryosurgery as developed by Marcove involves pouring of liquid nitrogen into the tumor bed. This approach revolutionized the treatment of some tumors such as giant cell tumor of bone, allowing intra-lesional resection to substitute the wide-resection method used up to that time. However, complications of this method of treatment are common, including nitrogen emboli, fractures of the bone due to extensive necrosis and damage to neurovascular elements. Dror Robinson, M.D., Ph.D. 1,2,* Mustafa Yassin, M.D. 1 Zvi Nevo, Ph.D. 2 1 The Department of Orthopedic Surgery Campus Golda Rabin Medical Center KKL 7 Str. Petach Tikwa, Israel 2 The Department of Clinical Biochemistry Sackler School of Medicine Tel Aviv University Tel Aviv, Israel A recent development in the field of cryosurgery has been the argon-based system allowing controlled formation of an ice-ball surrounding a metallic probe. The system is computer controlled and allows precise evaluation of the tumor bed interface as well as surrounding structures that need to be protected. Prior to application of this method in humans it is important to ensure that interface sterilization is indeed achieved using cryosurgery. To evaluate this question, a Swarm rat chondrosarcoma was used. Cell viability was assessed following ice-ball formation. Histological evaluation indicated that cell death occurs up to 5 millimeters from the ice-ball if temperatures of -40º Celsius at the metallic probe are achieved. A further evaluation was performed on samples obtained from patients during surgery. A minimum of two freezing cycles was shown to be necessary to achieve tissue viability similar to that of boiled tissue. Twenty-seven patients were operated to date using an argon-based cryosurgery system. The patients included 7 cases of grade I chondrosarcoma, 5 cases of giant cell tumor of bone, 14 cases of a metastatic lytic bone lesion and a single case of osseous-fibrous dysplasia. None of the patients suffered nerve injury during the operation. After a minimal follow-up period of 2 years only two of the surviving patients had a recurrence (a giant cell tumor of the proximal fibula, and the patient with the osseous-fibrous dysplasia whose tumor recurred as a frankly malignant adamantimoma). There were no pathological fractures. This method appears practical and allows close monitoring of the surrounding tissue to reduce the chances of recurrence. Key words: Cryosurgery, Argon-based system, Bone tumors, Chondrosarcoma, Giant cell tumor. * Corresponding Author: Dror Robinson, M.D. drorr@clalit.org.il robinson@bezeqint.net Abbreviations: Tetrazolium Salt 38-1-[(phenylamino)-carbonyl]-3,4-tetrazolium-bis(4-methoxy-6- nitro)benzenesulfonic Acid Hydrate, XTT. 371
2 372 Robinson et al. Introduction The improved results of multi-disciplinary treatment of bone tumors in recent years, allows consideration of the functional results of treatment. For most aggressive bone tumors the standard of treatment remains wide resection (1). However, especially in lesions close to the joints, functional results can be greatly improved by performing a marginal resection and relying on supplementary techniques to sterilize the tumorbone interface and lower the risk of tumor recurrence. The commonly acceptable method for supplementing tumor resection involves cryosurgery using liquid nitrogen. The classic technique was developed over thirty years ago and involves pouring liquid nitrogen into the tumor bed (2, 3). The potential problems with this technique are the risk of bone fractures due to uncontrolled thermal damage (4) and joint destruction due to cartilage necrosis. Other rare complications include nitrogen and bone marrow emboli causing arterial occlusion or pulmonary emboli (5). These complications led to an interest in developing a method for cryosurgery without the attendant risk to surrounding tissues. Concomitantly, advances in surgical techniques allow the performance of some bone tumor resections via a minimally invasive approach. As the use of liquid nitrogen involves the formation of large amounts of gas, classic cryosurgery requires large incisions and exposure of the entire tumor bed to air to prevent gas emboli. For minimally invasive surgery to be an option in bone tumor cryosurgery, it is essential to develop a method of cryosurgery that does not require release of gas, so that it could be employed via small incisions. Materials and Methods A recently developed medical device a allows in situ freezing of tumors by the formation of an ice-ball around a metallic probe. A surface probe with enlarged diameter allows freezing of a large cavity (Figure 1). Using multiple probes allows the merging of the ice-ball into a combined mass of the required shape to ensure freezing of the entire tumor bed. As the device allows real-time temperature measurements of both the tumor bed and surrounding tissues, thermal damage to surrounding tissues is avoided. The first objective prior to implementing this device in clinical practice has been the determination of the capability of the formed ice-ball to actually sterilize the tumor bone interface. One problem is that an important application of this device is expected in the treatment of cartilage tumors. However it is known that cartilage is relatively resistant to the deleterious effects of freezing and rapid thawing. In fact some cells survive in osteoarticular allografts at least from a morphological a (Cryohit, Galil Medical Technologies, point of view (6). Thus there is a definite risk that a single freezing session will not lead to total cartilage cell death. Other types of tumors might be more sensitive to freezing due to lack of matrix or less sensitive to freezing due to increased blood supply. Thus a protocol leading to cartilage cell destruction might be stringent enough for other tumors as well but detailed studies of other tumor types are needed. The Swarm rat chondrosarcoma model is a well described animal model of the human disease (7). Implantation of small pieces of the original tumors in a subcutaneous location, leads to rapid formation of a large subcutaneous tumor. The tumor consists entirely of cartilage and is large enough for probe insertion. Thus a model evaluating the effect of the formed ice-ball on malignant cartilage cells viability has been developed. Swarm s rat chondrosarcoma consistently yields a tumor mass consisting of cartilage tissue in the subcutaneous location. Subcutaneous tumors were implanted in rats under the skin of the back. The tumors were resected two months later and treated by cryosurgery. Average tumor size was 4 centimeters at this time. The tumor nodules were removed under sterile conditions after the rats were anesthesized and a cryoprobe of 3 millimeter diameter was inserted as well as two thermosensors at the edge of the tumors. This model is different from the clinical situation as no blood supply is available to the resected tumor and thus the moderating effect of the blood on tumor temperature is lost. Previous work has been published indicating that complete tumor cell ablation in hepatic tumors requires a minimum of -38º Celsius at the tumor edge (8). Thus the tumor masses were frozen twice each for five minutes. The control thermosensor was set to -40º Celsius. The system allows precise control of the ice-ball temperature using the control s thermosensor temperature as a guideline. The thawing process can proceed rapidly. Thus argon gas is used in this process. In the animal model used, the tumor masses were placed in 36º Celsius sterile saline to accelerate the thawing. Cell viability was monitored by two methods. Pieces of the frozen tumor were re-implanted in animals and the percentage of animals in which tumor growth occurred a month later was determined. In addition, cell viability studies were performed. Tiny morsels of approximately 2 cubic millimeters were cut from the periphery of the tumors. The morsels were placed immediately in sterile Dulbecco s growth medium supplemented by 10% fetal calf serum. Cellular viability was assessed using the XTT reaction. The specimens were placed in Dulbecco s minimal essential medium (DMEM) in a sterilecontainer. All specimens were transferred immediately to a tissue culture lab. Cell vitality was assessed by a reaction using the tetrazolium salt 38-1-[(phenylamino)-carbonyl]- 3,4-tetrazolium-bis(4-methoxy-6-nitro)benzenesulfonic acid hydrate (XTT). The XTT reaction allowed estimation of tissue viability. The XTT reagent kit for the determination of cell vitality is based on the reduction ability of tetrazolium
3 Cryosurgery of Musculoskeletal Tumors 373 salts by the mitochondrial enzymes (hydrogenases) of living cells, to form a soluble colored molecule a formazan dye, measured at 450 nm by an ELISA plate reader. The optical density is proportional to the number of living cells and their metabolic status (9). Each cylinder was divided into three pieces longitudinally. Each piece was weighed on an analytical balance. Explants were washed off their incubation medium, and 50 ml of medium containing the XTT reagent was added. It was incubated for 1 h at 37 ºC under 5% CO2 in air. The supernatants were transferred to another 96-well plate and read in the ELISA plate reader at 450 nm. The results were expressed as optical density per 100 mg of wet weight. The triplicates were averaged for further analysis. It should be appreciated that XTT underestimates the degree of cell death. This is due to the fact that dead cells might still contain active enzymes capable of interacting with the XTT reaction reagents. Thus, any results of XTT put a lower threshold on the degree of cell injury but the amount of interface destruction might in fact be much more extensive. At a later stage, patients treated by cryosurgery were assessed. The tissue was treated according to the cryosurgery protocol and later bone cylinders were removed for histological studies. In addition cellular viability of the interface was assessed using both XTT studies and cell cultures of the retrieved specimens. Clinical results were assessed after a minimum of two years. Patients were followed up regularly using an MRI scan (in the case of primary bone tumors), radiographs and bone scans every six months. Cryosurgery Protocol In Human Patients Operations were carried out without tourniquet application. Cryosurgery was begun after a thorough curettage of the lesion was performed. As the surgical exposure was small operations were performed under image intensifier control and total tumor ablation was demonstrated by filling the cavity with contrast solution. In situations that the bone was perforated, cellulose pads were used to plug the perforations prior to pouring in the contrast material. Some data is available (personal communication) that gel filling of the cavity shortens the time needed for achieving a freezing temprerature in the tumor bed. In our protocol, Esracaine1% gel was used due to availability. The cavity was filled to the brim with the gel after the cryo-probes were inserted and blood was suctioned out. Up to three3-mm probes and a 14-mm surface probe (developed by the company with the assistance of Prof. I. Meller of the National Orthopedic Oncology Unit, Tel Aviv Medical Center) were used. The number of probes used was determined according to the size of the lesion, its location and the surgical exposure. Three thermosensors were used routinely to monitor the procedure. One thermosensor was at the tumor-bone interface. It was the control thermosensor. It had a goal temperature of -40 ºC. These data relate to liver tumors; however, little information exists regarding bone tumors. Two other thermosensors were in a periosteal location (external thermosensors). The minimal temperature allowed in these thermosensors was 10 ºC. This combination of cryo-probes ensured in these cases an iceball filling the entire cavity in these tumors. The goal temperature was maintained for 2-5 min. Then rapid thawing using a helium channel allowed suctioning-off of the completely thawed gel. Thawing takes approximately 3 min (depending on the anatomy and size of the tumor). This procedure was repeated three times and the gel was replaced between cycles. Thermosensors reached a temperature of at least 25 ºC, prior to commencement of the next cycle. As detailed below 27 patients were treated according to this protocol. The defect was either packed with bone-graft substitute or with methyl-methacrylate. Patients were allowed weight-bearing as tolerated on the involved limb. Use of crutches was recommended for 6 weeks. Cast was not applied in any of the cases. Physiotherapy including active exercises to achieve maximal joint range of motion was used. Interface Viability Tumor-bone viability is influenced by the number of freezing cycles (10). A single freezing cycle is inadequate in the human clinical setting (Figure 4, 5, 6). This result contradicts the results achieved using the Swarm-rat chondrosarcoma model. It is our opinion that the difference is due to the cooling effect of blood flowing through the operated on limb. However, a basic difference between the tumor model used and human tumors could not be ruled out. Two freezing cycles appear adequate to achieve interface viability similar to boiled tissue. Results and Discussion The yield of chondrosarcoma formation in the rat model is over 95% when sterile un-frozen tumor morsels are implanted (n=30 in each group). Chondrosarcoma formation is adversely affected by tumor freezing. A single freeze cycle is appropriate in this model to prevent tumor formation in all animals (n=10). XTT results indicate that the tumor margins are not viable after freezing of the tumors to -40º Celsius. Figure 2 indicates a decrease in optical absorption signifying cell death in frozen specimens versus unfrozen ones. The decrease is apparent after the first freezing and there is no significant difference between the numbers of freeze cycles. According to these results it was felt that the treatment might be effective and a decision has been made to proceed with human patients. However, little information was available in the literature at the time
4 374 Robinson et al. regarding the optimal treatment protocol for using this device in bones. Freezing hepatic lesions (mostly metastases) has been studied previously and a required maximal temperature of the iceball of -38º Celsius was determined (8). However, at the time there was no knowledge in the literature regarding the correct protocol to use in bone tumors. A study was undertaken to assess the number of freeze cycles necessary to achieve interface sterility (10). Patients were operated according to a protocol garnered from the best available knowledge at the time. Figure 4: Difference between average viability ± standard deviation of tumor morsels of chondrosarcomas prior to and following several freezing cycles (expressed as optical density per 100 mg wet weight). Figure 1: In situ freezing via a mini-invasive methodology of a chondrosarcoma of the distal femur. Figure 2: Average viability ± standard deviation of tumor morsels (expressed as optical density per 100 mg wet weight). Figure 5: Live cartilage cell is seen following a single freeze-thaw cycle. Note that most of the lacunae are empty, but a single morphologically normal cell is seen. The specimen was removed from the remnant bone following curettage of a chondrosarcoma of the distal tibia (Hematoxillineosin stain, original magnification X200). Figure 3: An intra-operative report of temperatures achieved in the tumor and the surrounding tissues. The intra-tumor bed temperature is about -40º Celsius, and two cycles are recorded. Simultaneous recording of periosteal and intra-articular temperatures reveal a nadir of 10º Celsius in the surrounding tissues. Figure 6: No live cells are seen following two freeze-thaw cycles of the same tumor shown in Figure 5 (Hematoxillin-eosin stain, original magnification X200).
5 Cryosurgery of Musculoskeletal Tumors 375 Clinical Results Twenty-seven patients were operated to date using an argonbased cryosurgery system. The patients included 7 cases of grade I chondrosarcoma. Five cases of giant cell tumor of bone, 14 cases of a metastatic lytic bone lesion and a single case of osseous-fibrous dysplasia. There was one complication that could possibly be directly attributed to the cryosurgical procedure. One patient with chondrosarcoma of the distal femur suffered from severe muscle pain for two months after the surgery. A repeat MRI scan performed at this time demonstrated muscle damage presumably due to ischemia of the quadriceps. Possible cryogenic damage to the muscle could not be ruled out. The pain slowly resolved later. At the four-year mark there is no evidence of tumor recurrence in this patient. However, as methyl-methacrylate was used to fill up the defect in this case, thermal damage during cement setting is also a possibility in this case. Follow-up of the patients was carried out according to a standardized protocol. Patients underwent repeat radiographs at the six-weeks, three-months and six-months mark. The patients with primary bone tumors underwent an MRI scan at the six-months mark and yearly afterwards. Due to cost considerations MRI scans were not performed on metastatic patients. Tumor recurrence was noted in two cases (n=27) after a minimal follow-up period of 2 years in surviving patients. In one patient suffering from a giant cell tumor of the proximal fibula, recurrence occurred four years after the index procedure (Figure 7). The patient was treated by wide resection of the proximal fibula. Figure 7: A giant cell tumor of the proximal fibula (A) was treated by minimally invasive surgical procedure with curettage and cryoablation of the interface. Note the close proximity of the peroneal nerve (dissected and elevated on a rubber band). There was no nerve injury following this procedure. This tumor recurred four years later and required wide resection of the proximal fibula, resulting in peroneal pasly. In conclusion, it appears that using the argron system is a safe and effective method of augmenting marginal resection of aggressive bone tumors. The use of thermosensors is important as it allows real-time evaluation of the safety of surrounding tissue, thus preventing complications related to classical cryosurgery of musculoskeletal tumors. Recently, it has been suggested that this method is efficacious for use in sacral tumors as well and lowers the rate of neurological injury as compared to sacrectomy (11). The use of two-freezing cycles is essential as some viable tumor cells are left following a single cycle. The addition of a third freezing cycle does not appear to be warranted and was abandoned by our group. Acknowledgements The clinical cases were operated on by one of the authors (D. R.) at Assaf Harofe Medical Center from 1999 to The rat experiments were performed in 1999 at Assaf Harofe Medical Center. The authors have not received from any commercial entity any payments or any pecuniary, in-kind or other professional or personal benefits (collectively, the Benefits ), or any commitments or agreements to receive such Benefits, that were related in any way to the subject of the Work or the research that was conducted in connection with the research presented here. References Enneking, W. F., Spanier S. S. A System for the Surgical Staging of Musculoskeletal Sarcoma Clin. Orthop. 415, 4-18 (2003). Marcove, R. C. and T. R. Miller. The Treatment of Primary and Metastatic Localized Bone Tumors by Cryosurgery. Surg. Clin. North Am. 49, (1969). Marcove, R. C., Miller T. R. The Treatment of Primary and Metastaticbone Tumors by Repetitive Freezing. Bull. N. Y. Acad. Med. 44, (1968). Marcove, R. C., Weis L. D. Cryosurgery in the Treatment of Giant Cell Tumors of Bone: A Report of 52 Consecutive Cases. Clin. Orthop. 134, (1978). de Vries, J., Oosterhuis, J. W. Bone Marrow Embolism Following Cryosurgery of Bone: An Experimental Study. J. Surg. Res. 46, (1989). Caldroa, P., Donati, D. Histomorphologic Study of Explants of Massive Allografts: Preliminary Results. Chir. Organi. Mov. 80, (1995). Oegema, T. R., Jr., Hascall, V. C. Isolation and Characterization of Proteoglycans from the Swarm Rat Chondrosarcoma. J. Biol. Chem. 250, (1975). El-Shakhs, S. A., Shimi S. A. Effective Hepatic Cryoablation: Does It Enhance Tumor Dissemination? World J. Surg. 23, (1999). Scudiero, D. A., Shoemaker, R. H., Paull, K. D., Monks, A., Tierney, S., Nofziger, T. H., Currens, M. J., Seniff, D., Boyd, M. R. Evaluation of a Soluble Tetrazolium/Formazan Assay for Cell Growth and Drug Sensitivity in Culture Using Human and Other Tumor Cell Lines. Cancer Research 48, (1988). Robinson, D., Halperin N., Nevo, Z. Two Freezing Cycles Ensure Interface Sterilization by Cryosurgery During Bone Tumor Resection. Cryobiology 43, 4-10 (2001). Kollender, Y., Meller I., Bickels, J. Flusser, G., Issakov, J., Merimsky, O., Marouani, N., Nirkin, A., Weinbroum, A. A. Role of Adjuvant Cryosurgery in Intralesional Treatment of Sacral Tumors. Cancer 97, (2003). Date Received: January 24, 2004
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