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What's New in Musculoskeletal Oncology

¹ Department of Orthopaedic Surgery, Johns Hopkins School of Medicine, JHOC #5251, 601 North Caroline Street, Baltimore, MD 21287. E-mail address: kweber6{at}jhmi.edu

Specialty Update has been developed in collaboration with the Council of Musculoskeletal Specialty Societies (COMSS) of the American Academy of Orthopaedic Surgeons.

The author did not receive grants or outside funding in support of her research or preparation of this manuscript. She did not receive payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the author is affiliated or associated.

	Introduction

Top Introduction The Role of Interventional... Technical Advances in Limb... Advances in the Basic... Educational Opportunities Web Sites of Interest References

 
Advances in the diagnosis, treatment, and prevention of cancer have been rapid on both the basic and the clinical research front. This review will highlight recent discoveries and innovations and also will discuss refinements in established techniques in the field of musculoskeletal oncology. The dates and locations of future tumor-related meetings are included, and relevant web sites are listed.

	The Role of Interventional Radiology in Musculoskeletal Oncology

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The diagnosis and treatment of musculoskeletal tumors have been increasingly aided by techniques used by interventional radiologists. The ability to perform less invasive procedures often allows more efficient, less painful, and more cost-effective patient care. The trend toward the diagnosis of tumors on the basis of small tissue samples will be discussed. The role of arterial embolization of highly vascular tumors such as giant-cell tumor, multiple myeloma, and metastatic renal-cell carcinoma will be reviewed. Radiofrequency ablation has become the standard treatment for patients with osteoid osteoma, but this technique is being expanded to assist in the palliative treatment of patients with painful bone metastasis. Finally, minimally invasive techniques such as kyphoplasty, vertebroplasty, and acetabuloplasty may provide an alternative to major reconstructive surgery for patients with metastatic disease.

Needle Biopsy
The original method of obtaining a histologic diagnosis of a bone or soft-tissue tumor was open incisional biopsy. For most pathologists, this method remains the so-called gold standard for making a diagnosis because it provides the best chance of obtaining representative tissue. However, the trend at many major musculoskeletal tumor centers over the past ten to fifteen years has been to use smaller amounts of tissue for diagnosis. The benefits of needle biopsy include cost efficiency, patient convenience, and avoidance of the problems associated with poor open biopsy techniques. Smaller, more specialized biopsy tools have been developed, leading to an 85% to 90% rate of accuracy¹. Conscious sedation of the patient allows for outpatient protocols. Image guidance is used to identify a "high-yield" area of the tumor. Computerized tomography, ultrasound, and fluoroscopy can be used, depending on the location and type of tumor. The advances in the field of radiology include faster computerized tomographic scanners with better resolution. Three-dimensional reconstruction can be used to better define the exact location of the tumor. In the future, magnetic resonance imaging-guided biopsies will be performed, which should enhance the diagnostic accuracy of the procedure by focusing on the most viable sections of tumor.

Both fine-needle aspiration and core-needle biopsy can be performed on most bone and soft-tissue lesions. A fine-needle aspiration initially can be performed to confirm the presence of viable tumor, and then a larger core-needle biopsy can be performed and processed for permanent review the next day. The confirmatory diagnoses of metastatic carcinoma and recurrent sarcoma are particularly amenable to needle biopsy. In order for these methods to be effective as part of the multidisciplinary approach to the treatment of patients with musculoskeletal tumors, the cytopathologist and surgical pathologist must be well-trained to interpret small tissue samples. In addition, the surgeon, radiologist, and pathologist must be in constant communication. It is essential for the radiologist and pathologist to have knowledge of the possible diagnostic and therapeutic algorithms in order to provide the information that is needed by the clinician. Ideally, the biopsy and treatment of bone and soft-tissue lesions that are suspicious for malignancy should be performed by physicians who are experienced in the treatment of musculoskeletal tumors^2,3.

Advances in the development of new tumor markers, techniques of antigen retrieval, and methods of quality control have enhanced the sensitivity and reliability of diagnosis. New markers such as CK7, CK20, CA125, and thyroid transcription factor-1 (TTF-1) can help to determine the origin of an adenocarcinoma or aid in the recognition of other tumors. In patients who do not have an obvious primary site of disease on screening radiographs, these new markers can help to focus the search for, and guide the treatment of, the underlying lesion. CA125 is positive in patients with ovarian cancer, CK7 is positive in patients with breast and lung carcinoma, and CK20 is indicative of colon carcinoma if the CK7 marker is negative. Gastrointestinal stromal tumor (GIST) is positive for CD117 (c-kit) and CD34, while 75% of bronchogenic carcinomas are positive for TTF-1. With regard to melanoma, the standard S-100 protein has been augmented by HMB-45, MART-1 and Melan-A. Molecular techniques such as flow cytometry, fluorescence in situ hybridization (FISH) and polymerase chain reaction (PCR) are now being used to expand our knowledge of genetic alterations within tumors while also ensuring a more accurate diagnosis.

Arterial Embolization
Arterial embolization of hypervascular tumors has been used as an adjunct to surgical resection and, in some cases, has been used as the sole treatment for a tumor that is located in the spine or pelvis. When used in a preoperative setting, the embolization of feeder vessels to tumors such as metastatic renal-cell or thyroid carcinoma, giant-cell tumor, multiple myeloma, or aneurysmal bone cyst can result in a lower operative blood loss and a decreased need for intraoperative transfusions. This is particularly important in cases of large tumors that are located in sites where tourniquet control is not possible. Sun and Lang4, in a study of sixteen patients who had preoperative embolization for metastatic renal-cell carcinoma, found that the mean blood loss was significantly less for patients with >70% reduction in tumor vascularity than for those who had <70% reduction in tumor vascularity (460 compared with 750 mL; p < 0.01).

For large primary benign bone tumors (such as giant-cell tumor or aneurysmal bone cyst) that are located in the pelvis, spine, or shoulder girdle, embolization alone has been successfully used to halt growth of the tumor or, in some cases, to promote healing and mineralization of the mass. This may preclude the need for functionally debilitating surgery. Lin et al.⁵ reported the long-term results for eighteen patients in whom a sacral giant-cell tumor was treated with arterial embolization with use of Gelfoam and coils. Repeat embolizations were performed on the basis of clinical symptoms and the vascularity of the tumor. Fourteen of eighteen patients had a favorable response, with reduction of pain and neurological improvement, after a median duration of follow-up of 105 months.

Advances in interventional radiology techniques also have been used for neoadjuvant chemotherapy administration in patients with osteosarcoma involving an extremity. Several major centers in the United States utilize this approach for the administration of intra-arterial cis-platinum. The rationale is that this approach has a regional pharmacokinetic advantage over intravenous treatment. Maximizing local delivery of the drug theoretically enhances the local response rate while still allowing a high-enough concentration of the drug in the draining vein to provide a systemic effect on micrometastasis. There have been conflicting reports in the recent literature regarding the effect on local recurrence and overall survival. Researchers at the MD Anderson Cancer Center reviewed 155 intra-arterial infusions of cis-platinum in forty-two patients from 1999 to 2002 (unpublished data). The procedure was found to be safe, with no reported instances of skin necrosis, thrombosis, infection, neuropathy, or compartment syndrome. There were seven painful burns (in six patients) consisting of skin erythema and induration. The long-term results related to local recurrence and survival in this group of patients are pending.

Radiofrequency Ablation
The use of radiofrequency ablation to treat osteoid osteoma began ten years ago, and there is now an accumulated experience with patients who have had long-term follow-up⁶. These small, painful, benign bone tumors traditionally have been treated with either prolonged use of nonsteroidal anti-inflammatory medications or surgical resection. The surgical procedures often were extensive as the nidus was difficult to identify. Because the lesions frequently are located in weight-bearing bones, patient activities were restricted postoperatively and fractures were a known complication of the procedure. In addition, incomplete removal led to local recurrence of the painful lesion. Radiofrequency ablation provides a percutaneous, computerized tomography-guided alternative for removal of lesions and has been associated with a low complication rate. It is performed as an outpatient procedure, and the patient can bear weight as tolerated immediately after the ablation. Rosenthal et al.⁶ reported on 263 patients who had had 271 radiofrequency ablation procedures for the removal of an osteoid osteoma over a period of eleven years. The rate of complications was <1%, and successful ablation was achieved in 91% of the patients who had a primary lesion. Of those who had a recurrent osteoid osteoma, 60% were successfully treated with a second radiofrequency ablation procedure.

More recently, radiofrequency ablation has been used for the palliative treatment of painful bone metastasis. This procedure provides an alternative or adjunct to radiation or surgery and can be performed in conjunction with fine-needle aspiration to confirm the diagnosis. Callstrom et al.⁷ recently described the mechanism of pain relief after radiofrequency ablation. Specifically, the procedure results in physical destruction of sensory nerve fibers involving the periosteum and cortex in addition to mechanical decompression of the tumor volume, which, in turn, decreases the stimulation of nerve fibers. In addition, radiofrequency ablation destroys tumor cells that produce nerve-stimulating cytokines such as TNF- and various interleukins while also inhibiting osteoclast activity.

Goetz et al.⁸, in a recent multicenter study, reported on forty-three patients with bone metastases who were managed with radiofrequency ablation. The mean tumor size was 6.3 cm, and the majority of lesions were located in the pelvis or sacrum. Seventy-four percent of the patients had had prior radiation treatment, and all patients either had failed to respond to such treatment or were considered to be poor candidates for radiation or narcotic medication. Radiofrequency ablation was associated with a clinically important benefit (a 2-point drop in the "worst pain" parameter) in 95% of the patients.

Related percutaneous techniques of kyphoplasty and vertebroplasty have been successfully used to relieve pain in patients with spinal compression fractures resulting from osteoporosis, multiple myeloma, and metastatic disease. Multiple studies in the recent literature have reflected the popularity of these techniques⁹.

	Technical Advances in Limb-Salvage Surgery

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Locked Plating Systems
The development of the locked plating system for internal fixation has important applications in the treatment of bone tumors. This system merges locking screw technology with standard plate-fixation techniques. The locking screws provide the ability to make a fixed-angle construct, which is important when treating bone of poor quality. The screws function as multiple small blade-plates, rather than relying on compression of the plate to the underlying bone, to achieve secure fixation. Koval et al.¹⁰ reported that a locking condylar plate on the distal part of the femur provided significantly greater fixation stability during axial loading than did a standard condylar plate or blade-plate.

There are several potentially useful applications of the locking plate technology in musculoskeletal tumor surgery, although no large series has been published to date. Documented complications such as nonunion and hardware failure are not uncommon when an intercalary allograft is used for reconstruction after resection of a primary malignant diaphyseal tumor, and a stable construct is necessary to facilitate host-allograft healing. The locking plate system can provide stable fixation when used alone or when combined with a vascularized fibular graft. More importantly, unicortical screw fixation is available with the locking plate systems and allows fewer holes to be placed in the allograft. This may decrease the chance of allograft resorption or fracture in these areas. In addition, the locking plate can be used for prophylactic fixation of an impending fracture secondary to bone metastasis in the distal part of the femur or proximal part of the tibia.

Uncemented Stem Fixation
Uncemented fixation of tumor prostheses has been employed commonly in Europe but has not been the procedure of choice in the United States. The technique has been popularized for total hip arthroplasty in patients with degenerative joint disease, especially in the younger population. In recent years, there have been several intermediate-term and long-term reports on uncemented fixation of tumor megaprostheses. Donati et al.¹¹ reported on twenty-five patients who had received an uncemented proximal femoral modular prostheses after tumor resection. After more than ten years of follow-up, only four patients had required revision but more than two-thirds of the patients had evidence of stress-shielding. Mittermayer et al.¹², in a study of 251 patients who had received an uncemented Kotz tumor prosthesis for reconstruction of the femur or tibia, reported that twenty-one patients required revision because of aseptic loosening. The chance of avoiding aseptic loosening at ten years was 96% for patients who had received a proximal femoral implant, 76% for those who had received a distal femoral implant, and 85% for those who had received a proximal tibial implant. The first signs of loosening were noted radiographically at a mean of twelve months. These results are comparable with or better than those in reports of aseptic loosening of cemented megaprostheses¹³, although no direct comparison studies have been completed to date.

A novel spring-loaded, titanium-alloy uncemented implant was recently developed to address the problem of loosening secondary to stress-shielding in patients managed with tumor prostheses¹⁴. The Compliant Prestress segmental replacement and fixation system initially was tested in a sheep model and now is being used in a multicenter clinical trial. The Compliant Prestress device has a porous-coated surface that is compressed against the cortical osteotomy site at the host-bone surface with Belleville washers that are tightened over an 8-cm intramedullary traction bar. An internal spring can create predetermined forces of 1800, 2700, or 3600 N at the bone-implant interface. In the sheep model, a circumferential buttress of new bone was noted at the prosthesis-bone interface and bone ingrowth was identified on retrieval studies, implying stress transference through the cortex. At the meeting of the Connective Tissue Oncology Society that was held in Barcelona, Spain, in November 2003, twenty-six patients who had been treated in the United States with a Compliant Prestress device following a primary or revision oncologic distal femoral resection were compared with a matched group of twenty-six patients who had been treated in the United Kingdom with a traditional cemented intramedullary stem. After a mean duration of follow-up of 2.2 years for the group treated in the United States and of 1.8 years for the group treated in the United Kingdom, there had been only one device-related prosthetic failure in each group. Additional follow-up is necessary, but this unique, uncemented compression system may improve implant survival in young patients with bone sarcomas who require resection and reconstruction of weight-bearing joints.

Expandable Prostheses for Pediatric Patients
Another challenge for the orthopaedic oncologist is the treatment of skeletally immature patients in whom the tumor location necessitates resection of the physis. Continued growth of the contralateral limb often results in a substantial limb-length discrepancy, depending on the years of remaining growth. Therefore, many patients whose anticipated limb-length discrepancy is >4 cm may undergo amputation or rotationplasty. If prosthetic reconstruction is performed, an expandable device is necessary to allow for gradual equalization of limb lengths by the completion of growth. The early expandable devices had a high rate of failure at the expansion mechanism, necessitating additional operations and resulting in an increased chance of prosthetic infection. There has been a trend toward minimally invasive expandable devices over the past ten years. Most recently, a novel, noninvasive, expandable device has become available with energy stored in a compressed spring that is released in a controlled fashion during application of an electromagnetic field. The lengthening is performed in an outpatient setting. The Phenix prosthesis (now manufactured as the Repiphysis by Wright Medical Technology, Arlington, Tennessee) is a fixed-hinge, titanium implant with the capability to expand that depends upon the length of bone resection as well as the anticipated limb-length discrepancy at skeletal maturity. During application of an electromagnetic field that heats to 130°C, the polyethylene around a titanium tube melts. This allows a controlled slide and elongation of 6 to 20 mm with no undue heating of the surrounding tissues.

The early multicenter experience with the Phenix implant has been promising. Neel et al.¹⁵ reported on eighteen prostheses that were implanted in fifteen children with osteosarcoma of the distal part of the femur or proximal part of the tibia. Sixty expansions were performed, with 97% occurring in an outpatient setting. After a mean duration of follow-up of 21.5 months, Musculoskeletal Tumor Society functional scores were a mean of 90% (27 of 30 points). Eight revisions for stem fracture or loosening were required. There have been subsequent modifications of the prosthesis, and more recent data were presented at the Twelfth International Symposium on Limb Salvage (ISOLS), held in Rio de Janeiro, Brazil, in September 2003. From 1999 through 2003, twelve patients had placement of the Repiphysis device and were followed for a mean of twenty-eight months. Fifty-one expansions in eleven patients were performed, with an average lengthening of 8.3 mm per expansion. One prosthesis was revised after a fall, but no aseptic loosening was noted in any patient. The mean ISOLS functional score was 96%. This novel technique may have more widespread application in the treatment of limb-length inequality or spinal deformity.

	Advances in the Basic Understanding of Musculoskeletal Tumors

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The recent literature was reviewed along with the tumor-related national and international meeting abstracts from 2003. Several interesting studies that were presented or published had diagnostic or treatment implications for patients with bone or soft-tissue sarcomas. Recent basic-science studies have focused on the association of different growth factors, cytokines, or enzymes with specific tumors. Data also are being generated from microarray analyses, and the daunting task in the next ten to twenty years will be to synthesize this information into something that is clinically meaningful. Despite the association of certain factors with specific tumors, extensive multicenter cooperation will be necessary in order to collect sufficient data to develop real guidelines for molecular diagnosis and targeted treatment. A focus on basic mechanisms of how sarcomas proliferate and metastasize may provide new avenues for treatment.

It has been proposed that an imbalance in the proteolytic cascade involving matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) may play a role in the development or progression of malignancy. Benassi et al.¹⁶ studied the activity of MMP2 and MMP9 as well as their inhibitors, TIMP2 and TIMP1, respectively, in patients with high-risk soft-tissue sarcomas. The TIMP activity was weak or nonexistent and MMP activity was high in the majority of sixty-nine biopsy tissue samples tested with zymography and immunohistochemistry. The plasma concentration of TIMPs was significantly lower in fifty-three patients with soft-tissue sarcoma than in the fifty-six control patients (p = 0.0001). The authors suggested that identifying the levels of the tissue inhibitors of MMPs might allow better selection of patients with aggressive tumors who have a poor prognosis. These patients would be candidates for clinical trials with experimental therapies.

At the Twelfth International Symposium on Limb Salvage in September 2003, it was reported that expression of vascular endothelial growth factor in the tumors of patients with both Ewing sarcoma and chondrosarcoma was a negative prognostic indicator. The expression of this factor is associated with angiogenesis and aggressive growth of many tumors, making it a potential therapeutic target. At the same meeting, investigators from Australia used a mouse tibial injection model to demonstrate that the hyaline cartilage of the epiphyseal plate and joint surface was resistant to local invasion by osteosarcoma cells, irrespective of tumor size. The tumors were positive for vascular endothelial growth factor and negative for the anti-angiogenic factor, pigment epithelium-derived factor. In contrast, there was high expression of pigment epithelium-derived factor in the upper layers of the growth plate. The investigators hypothesized that the balance between pro-angiogenic and anti-angiogenic factors plays a role in the resistance of hyaline cartilage to invading osteosarcoma cells. This may partially explain the clinical observation that while tumors occasionally may cross the growth plate, they do not cross the articular surface unless there has been a fracture.

Holzer et al.¹⁷, in a clinical study, determined the bone-mineral density of forty-eight long-term survivors of high-grade osteosarcoma who had been managed with a specific international protocol that included high-dose methotrexate. The mean age of the patients was thirty-one years. Dual-energy x-ray absorptiometry of the spine and the contralateral femur was performed after a mean duration of follow-up of sixteen years. Ten patients were found to have osteoporosis, twenty-one were found to have osteopenia, and seventeen had normal bone density. Eighteen patients sustained a fracture after chemotherapy and had low bone-mineral density levels at all measured locations. That study underscores the importance of long-term evaluation of patients with osteosarcoma. Patients should have follow-up bone-mineral density studies and should be counseled regarding possible treatments or activity modifications.

Grier et al.¹⁸, in an important study of 518 patients with Ewing sarcoma that was published in the New England Journal of Medicine, noted that the addition of ifosfamide and etoposide to the standard regimen of doxorubicin, vincristine, cyclophosphamide, and dactinomycin was effective in patients with localized disease. The five-year event-free survival rate and the overall survival rate were significantly improved in the experimental therapy group (p = 0.005 and p = 0.01, respectively). The results of that work are now reflected in the design of current treatment regimens for patients with Ewing sarcoma.

Conversely, a clinical study performed at the Rizzoli Institute in Italy evaluated a dose-intensive chemotherapy regimen in patients with osteosarcoma and found no improvement in the histologic response to chemotherapy, the rate of local recurrence, or the five-year event-free and overall survival rates when increased doses were used¹⁹. From 1993 to 1995, 175 patients with nonmetastatic osteosarcoma of an extremity were treated with neoadjuvant methotrexate, cisplatin, doxorubicin, and ifosfamide. From 1995 to 1999, 196 similar patients were treated with increased doses of the same agents. The postoperative treatment was the same in both groups, with a longer course for patients with poor necrosis rates. A lower pretreatment serum alkaline phosphatase level and a better histologic response to chemotherapy were each predictive of an improved five-year rate of event-free survival. The results of these two studies might suggest that the histologic response to chemotherapy is a result of the inherent chemosensitivity of the particular tumor. Rather than increasing doses of currently used drugs, innovative therapies are necessary to further increase the survival of children with malignant bone tumors.

	Educational Opportunities

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Upcoming meetings will provide the latest information related to the treatment of patients with primary bone and soft-tissue tumors and those with metastatic disease. The American Society of Clinical Oncology (www.asco.org) is focused on clinical research and the latest clinical trials for all types of cancer. The next meeting will be held on June 5 through 8, 2004, in New Orleans, Louisiana. The annual meeting of the Musculoskeletal Tumor Society (www.msts.org) will be held on July 22 through 24, 2004, in Long Beach, California. The American Society for Bone and Mineral Research (www.asbmr.org) is a smaller group of researchers and clinicians focused on disorders of bone, including osteoporosis and cancer. The next meeting will be held on October 1 through 5, 2004, in Seattle, Washington. The International Skeletal Society (ISS) (www.international-skeletalsociety.com) is an organization comprising pathologists, radiologists, and surgeons interested in musculoskeletal tumors and related diseases. The next meeting will be held on October 6 through 9, 2004, in St. Julian's, Malta. The Connective Tissue Oncology Society (www.ctos.org) is a multidisciplinary group of orthopaedic surgeons, surgical oncologists, medical/pediatric oncologists, pathologists, and radiation oncologists interested in the treatment of patients with sarcoma. The next meeting will be held on November 11 through 13, 2004, in Montreal, Quebec, Canada. In addition, the Musculoskeletal Tumor Society participates in Specialty Day at the annual AAOS meeting, which will be held on February 23 through 27, 2005, in Washington, DC.

	Web Sites of Interest

Top Introduction The Role of Interventional... Technical Advances in Limb... Advances in the Basic... Educational Opportunities Web Sites of Interest References

 
Patient Education

• American Cancer Society (www.cancer.org)
  
• National Cancer Institute (www.cancer.gov)
  

Resident Education

• www.bonetumor.org
  
• www.ctisus.com
  

	References

Top Introduction The Role of Interventional... Technical Advances in Limb... Advances in the Basic... Educational Opportunities Web Sites of Interest References

 

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