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Overview of Limb Salvage Surgery (Limb Sparing Surgery for Bone Tumors)

Limb Salvage Surgery for Extremity Sarcomas
Henry DeGroot III, M.D. and Bruce Ellison, M.D.

Musculoskeletal Oncology Service
Department of Orthopedics and Physical Rehabilitation
University Of Massachusetts Medical School
Umass-Memorial Medical Medical Center
Worcester, Massachusetts

Introduction
Limb salvage surgery includes all of the surgical procedures designed to accomplish removal of a malignant tumor and reconstruction of the limb with an acceptable oncologic, functional, and cosmetic result. In the recent past, most sarcomas were treated by amputation. 1,2 Tumor recurrence, metastasis, and a generally dismal prognosis were a powerful deterrent to progress in treatment. Limb salvage surgery has all but replaced amputation as the treatment of choice for sarcomas of the extremities. 1 This dramatic change came about as the result of two important developments: effective chemotherapy 35 and precision imaging techniques. 69 In the early 1970’s, new anti—neoplastic drugs such as adriamycin and methotrexate were introduced, and remarkable improvements in the prognosis for some sarcomas were seen.2’3 In the late 1970’s, the development of CT and MRI allowed doctors to more precisely define the anatomic extent of the tumor, making it easier to remove the sarcoma without resorting to amputation. Today, up to 85% of sarcomas in the extremities are treated with limb salvage surgery. 3,68
Early Management and Referral
A successful limb salvage depends on a well—coordinated and timely series of events that begins with the first physician to see the patient. The physician who suspects a malignant tumor should do a thorough history and general examination. The basic work-up should include high quality plain radiographs for bone lesions10 and an MRI for soft tissue tumors.’0’11
If these basic investigations reveal a potential bone or soft tissue sarcoma, the next step would be to initiate a referral to a specialist, preferably by phone or by personal contact. The referring physician should not undertake an extensive work—up until this contact has been made. The choice and sequence of imaging and diagnostic tests should be carefully coordinated between the two physicians.
Evaluation of the images by an experienced orthopedic oncologist or musculoskeletal radiologist can often narrow the differential diagnosis through one or two entities. Sometimes the tumor may be found to be a benign or post—traumatic process, and multiple expensive tests may never be needed. Biopsy is not a part of the initial management of these lesions and is usually the last step in the work—up. Except in rare instances, the biopsy should be performed by the surgeon who will be doing the definitive surgery. 11, 13 Biopsy-related complications have been shown to lead to an amputation being required in cases where the limb might otherwise have been salvaged.12’13 Prompt, appropriate care in the first stages of the disease has an enormously positive impact on overall patient satisfaction and outcome.
Work-up
The next step in the process is the specialist’s evaluation. If the tumor is found to be aggressive or malignant, a complete staging work-up is arranged, and the team of physicians who will collaborate in the patient’s care is assembled. Typically, this multidisciplinary team includes orthopedic, surgical, medical and radiation oncologists, as well as a musculoskeletal radiologist, a pathologist, and a clinical psychologist or social worker. 14-16
For bone and soft tissue sarcomas, the basic staging work—up should include high quality plain radiographs of the affected bone or soft tissue area, a magnetic resonance imaging study of the entire tumor and nearby anatomic structures, a computed tomography scan of the chest, a whole body technetium bone scan, and a biopsy of the tumor.10”4 The best location and method for the biopsy is selected based on the results of the staging work—up, and the experience and skills of the care team. The biopsy site must be carefully planned and located along so-called “limb—salvage lines” (Figure 1), so that the entire biopsy track can be excised en bloc with the tumor if limb salvage surgery becomes necessary.15 Biopsy is a technically simple procedure but a complex cognitive skill that requires thoughtful consideration of every diagnostic possibility.12
Staging
Both imaging studies and biopsy results are used to stage bone and soft tissue sarcomas according to the system devised by William Enneking,10’14 and modified and adopted by the Musculoskeletal Tumor Society and later, the American Joint Committee for Cancer.’0 The system combines the biopsy findings with the local extent of the tumor to determine the stage. The biopsy material is examined for malignant features and the histologic grade is determined. The imaging studies are examined to determine the local extent of the tumor (Figure 2).
Staging the tumor allows the treatment team to plan and implement any appropriate preoperative chemotherapy or radiation treatments, and allows the surgeon to begin planning the limb salvage procedure. Preoperative chemotherapy and radiation therapy may facilitate limb salvage surgery by making a previously unresectable tumor amenable to surgery.13
Patient Education
The preoperative treatment period provides an opportunity for the surgeon to meet with the patient and family to discuss the choice of surgical treatment. The patient and the patient’s
family should be given the opportunity to participate in the decision—making process to the greatest extent possible. Treatment by amputation remains a viable and sometimes preferable option and should be openly discussed with the patient in an unbiased manner. The physician should try to help the patient understand what effect the treatment will have on the patient’s lifestyle and mobility in practical terms. When the patient and the family are fully informed and participate in the choice of treatment, they are much more likely to be satisfied with the ultimate outcome, even if complications and problems arise. 17
Indications for Limb Salvage Surgery
Currently, every patient with a malignant tumor of the extremity should be considered for limb salvage if the tumor can be removed with an adequate margin and the resulting limb is worth saving. An adequate margin is one that results in an acceptably low rate of local recurrence of the tumor. A limb worth saving needs an acceptable degree of function and cosmetic appearance with a minimal amount of pain, and needs to be durable enough to withstand the demands of normal daily activities. Balancing these sometimes conflicting requirements is what makes limb salvage surgery a complex, difficult, and rewarding process.
The patient’s prognosis has a limited impact on the decision to perform limb salvage surgery. The ability to predict the survival of any particular patient is quite limited, and some of the most valuable information is unavailable until after the limb salvage procedure is completed.2’3’11’18 While there are patients with advanced disease who clearly will not benefit from limb salvage, there is no justification for limiting the limb salvage process based only on the patient’s prognosis.
In selected cases, limb salvage can be combined with metastasectomy. For patients with uncontrollable disease, limb salvage should be considered if the surgery can be accomplished
with minimum morbidity and rapid return to function. These patients can enjoy relief from pain, improved quality of life, and intact body image that limb salvage can offer, even if they may not survive long—term.
Treatment of a sarcoma in an extremity by modern multidisciplinary techniques is an enormously costly process, and there is no consensus as to whether limb-salvage surgery is more or less expensive than treatment by amputation alone. In 1995 the Musculoskeletal Tumor Society found no significant difference in cost between various techniques of limb salvage and amputation, although the participants agreed that true cost data were not available to validate their findings.
Barriers to Limb Salvage
Barriers to limb salvage include poorly placed biopsy incisions, major vascular involvement, incasement of a major motor nerve, pathological fracture of the involved bone, and others.19~22 These adverse factors should not be viewed as absolute contraindications. 21,23,26
The so-called “three strikes rule” is a simple but helpful method of assessing the feasibility of limb salvage in any particular case. Each “strike” represents involvement of one of the four key components needed for a viable limb: the bone, the nerves, the vessels, and the soft tissue envelope. If just one or two of these key components must be resected in order to obtain an adequate margin around the tumor, then the limb may be salvageable. If three of these key components are involved, limb salvage is probably not worth considering.
Surgical Resections and Reconstructions
The cornerstone of a limb salvage procedure is a complete resection of the tumor with an adequate margin. Margins can be defined as intralesional, marginal, wide, and radical (Figure 3). An intralesional margin is created if the tumor is entered or cut into at any point during surgery. A marginal margin is created when the surgical dissection extends into or through the abnormal, reactive tissues that surround the tumor but are not actually a part of the tumor, the so-called “reactive zone.” A wide margin is created when the reactive zone is not entered, but instead the dissection is through entirely normal tissues, and a cuff of normal tissue is left on all sides of the tumor. A radical margin is created if the surgeon resects the entire bony or myofascial compartment or compartments containing the tumor.14
Exactly what constitutes an adequate margin in any particular case remains controversial.14 For high grade sarcomas, a wide margin is considered adequate and will achieve successful control of the primary tumor approximately 95% of the time, whereas marginal or intralesional margins are associated with frequent local recurrence and poor outcomes. 7,28 In low grade tumors or in high grade tumors where preoperative radiation therapy has been given, a marginal margin 27 may be adequate. In practice, the line between a wide and a marginal margin is sometimes difficult to define as the surgeon strives to control the tumor while still leaving the patient with a useful limb.
After completion of the tumor resection, the surgeon must reconstruct the resulting surgical defect. For most soft tissue tumors, a complex reconstruction is not required. occasionally, the reconstruction or substitution of a segment of artery or nerve may be required. The surgeon must eliminate potential deadspace and transfer tissues if necessary to allow an effective closure. Many bone sarcomas occur in the metaphyseal portion of the bone, so that the typical resection involves the whole proximal or distal part of the bone (Figure 4). If the joint is not contaminated by the tumor, an intra—articular resection is performed through the joint. If the joint is contaminated, then an extra—articular resection is required, taking the entire joint and joint capsule, and cutting through the uninvolved bone on the other side of the joint to achieve a wide margin. For tumors that involve the diaphyseal portion of a bone, an intercalary resection and reconstruction can be performed that saves the joints at either end.
Small resected segments of bone should be reconstructed using autogenous bone from the patient’s iliac crest or other sites, but the available supply is strictly limited. In most cases the excised segment of bone must be replaced, either by a large internal prosthesis, a segment of allograft bone, a composite of an allograft and a prosthesis, or by other methods.
Megaprosthesis
A megaprosthesis is a large metallic device designed to replace the excised length of bone and the adjacent joint (Figure 5). Modular designs are available for the most common uses in the femur, tibia, and humerus that allow the surgeon to assemble the prosthesis intra—operatively to accommodate the needs of a particular patient. Custom prostheses are available for special applications.
The prosthetic joint must be of a modified hinge design to substitute for the stability normally provided by the capsular and ligamentous structures that were sacrificed by the resection. The prosthesis is normally fixed to the host bones with polymethylmethacrylate cement. Special attention is paid during closure to ensure that the prosthesis is fully covered by a healthy soft tissue envelope. 22,24
The advantage of a megaprosthesis is that they are available “off the shelf” in a wide range of sizes and features to suit many reconstructive needs. Fixation with cement gives the 15 reconstruction immediate stability and allows rapid mobilization of the patient following surgery.
Regardless of the method of fixation to the host bone, the prosthesis may loosen over time. Mechanical wear of the polyethylene bearing surfaces and the metal joints between segments of a prosthesis can lead to early or late failure of the reconstruction. The reattachment of muscle tendons to the prosthesis is difficult and can lead to loss of motor power or full range of motion of the joint.22’29 When these implants fail, revision procedures have generally been successful after implantation of a new prosthesis.
Allografts
The allograft is harvested under sterile conditions, and the cartilage is protected with a cryoprotectant. 30 The graft can be stored indefinitely at -80 degrees C. 3l and is made available after bacteriologic and viral control.4’30’31 No suppression of the host’s immune response is necessary. After the tumor resection, an allograft that has been carefully size-matched to the intended recipient is cut to the appropriate shape (Figure 6). The shaft of the allograft is fixed to the end of the host bone with a bone plate or an intramedullary rod. For osteoarticular allograft reconstructions of a joint, an allograft with intact joint capsule and ligaments that matches the articular size and geometry of the resected specimen as closely as possible is selected. Heavy, non—absorbable sutures are used to join the capsule and ligaments of the allograft to their counterparts on the host bone. Muscle insertions are repaired to the stumps of tendons on the allograft.
If a sufficient inventory of allografts is available, a substitute for virtually any excised bone segment can be obtained. The attachment of muscle insertions is more successful in allografts than in prostheses, yielding better function in some sites. Initial enthusiasm for allografts has been tempered by a variety of problems as experience has accumulated.32’33 While it was initially hoped that massive allografts would become fully incorporated into the host, retrieval data show that only a small percentage of the allograft actually becomes revascularized, while the rest remains necrotic.34’35 Rather than a biologic replacement for the excised bone segment, the allograft functions as a biologic spacer.19’35 Massive allografts are susceptible to fractures and infection,32 and adjuvant treatment with chemotherapy and radiation increase the complication rate.31’32 The articular cartilage is subject to degenerative changes.31’36 An additional concern is the potential for the transmission of bacterial or viral disease.37’38 Although numerous problems continue to limit the success of allograft reconstructions, they remain a viable choice for selected uses,39 especially in the upper extremity, for intercalary resections, 40 and for patients who will not need chemotherapy.
Alloprosthetic Composite and Others
Some surgeons prefer to use a composite of an allograft and a prosthesis for certain limb salvage reconstructions. (Figure 7). An appropriate allograft is selected and implanted to replace the segment of bone resected. 33 The articular surfaces of the graft are excised and replaced using conventional techniques of total joint arthroplasty. The allograft provides a source of bone stock and a site for tendon insertions, while the prosthesis provides a reliable and stable articulation and some support for the allograft. The surgeon can customize the implant for any particular need.
Other techniques are available for special circumstances. An intercalary bone defect can be filled with autograft or spanned with a vascularized free fibula, 41 or by a new experimental technique using the concept of distraction osteogenesis as popularized by Ilizarov and others.42
Limb Salvage Procedures in the Upper Extremity
The location of the tumor has an important impact on the choice of technique for limb salvage. A reconstruction that combines the mobility and stability of the shoulder joint required for optimal upper extremity function is a major technical challenge.
The functional results of limb salvage reconstructions involving the shoulder joint depend largely on the extent of the resection. 43,45 Osteoarticular allografts of the proximal humerus allow effective reattachment of the rotator cuff and deltoid muscles, and demonstrate better stability, function, and overall motion. Use of a megaprosthesis for reconstruction of this type of surgical defect is popular, but has been associated with a significant rate of shoulder instability.45
Patients whose tumor invades the shoulder joint require an extra—articular resection that includes the proximal humerus and all or part of the scapula. If enough of the scapula is intact, a scapulohumeral arthrodesis of the shoulder can be performed using an allograft to bridge the bony gap (Figure 8). This type of reconstruction can lead to an excellent functional result.
The distal radius is another relatively common site for aggressive bone tumors. The ipsilateral fibula may be used as vascularized or non—vascularized autograft to replace the distal radius and may be the best method if available.41 Allograft reconstructions of the distal radius can yield favorable functional results.46
Sarcomas in the hand are associated with a relatively high rate of local recurrence and a worse overall prognosis.47 A wide resection is paramount, and amputation should be considered if a reasonable amount of function cannot be spared. Reconstructive efforts are generally limited to maximizing the function of the remaining hand structures.
Limb Salvage Procedures in the Lower Extremity
The proximal thigh is the most common locations for many soft tissue sarcomas, and the proximal femur is a frequent location of bone sarcomas. The proximity of the femoral vessels, as well as the peritoneum and retroperitoneum, make the surgical treatment of soft tissue tumors a challenge in this location.4850 Recurrence is a problem in large, proximal soft tissue tumors. Despite these challenges, limb salvage is a preferable alternative to treatment by amputation, which would
require a hemipelvectomy. Most soft tissue sarcomas do not require a complex reconstruction provided the potential dead space can be eliminated and sufficient soft tissue coverage can be achieved. Aggressive use of local tissue transfers or vascularized free tissue grafts is warranted.20
Bone sarcomas in the proximal femur require the resection and reconstruction of the hip joint and proximal femur. The results of megaprostheses and alloprosthetic composites used for the proximal femur are both favorable.33 Proximal femoral megaprostheses become prone to dislocation if the entire capsule of the hip joint is resected. In that case, a bipolar or monopolar prosthesis is more stable than a total joint arthroplasty. The osteoarticular allografts used to replace the proximal femur are prone to frequent fractures51 and results are poor.
The distal femur is a common site for primary bone sarcomas. The success rate of osteoarticular allografts used to reconstruct the distal part of the femur for sarcomas ranges from 27% to
73%. 41,51,53 Initially favorable results have deteriorated with longer follow—up. Failed osteoarticular allografts can be successfully converted to total knee arthroplasty with a favorable overall rate of limb salvage.26
Allograft—prosthetic composites have also been used to reconstruct the distal femur. The early results show that the technique has promise, and the outcomes are at least comparable with those of other reconstructive methods, while some of the more troublesome complications are less frequent.54
Tumors around the knee are also a difficult reconstructive challenge for those surgeons who prefer to replace the bone with a megaprosthesis. 8,55,56 Studies have reported complication rates as high as 55%. 55 Despite these problems, many surgeons prefer to use a megaprosthesis for the reconstruction of the distal femur due to their predictably good function, immediate functional restoration, the avoidance of delay in resumption of chemotherapy in high-grade sarcomas.Reconstruction of the proximal tibia is complicated by the relatively thin soft tissue envelope present in the area, the proximity of the neurovascular structures to the bone, and the need to restore the insertion of the extensor mechanism to achieve satisfactory function.
When a megaprosthesis is selected, routine transfer of the medial gastrocnemius is recommended to help provide coverage for the prosthesis and enhance the healing and function of the extensor reattachment. Osteoarticular allografts generally provide better extensor function than prostheses, although only small series and short follow—up have been reported, and results have been seen to deteriorate with time.9 An alloprosthetic composite is a favorable technique for the proximal tibia, due to the superior function of the extensor mechanism attachment, and the fact that the stem of the prosthesis supports the allograft and helps prevent fractures. Fixing the prosthesis to the graft with antibiotic-impregnated polymethylmethacrylate cement may reduce the incidence of infections.
For sarcomas that occur in the lower part of the leg, ankle,and foot, the probable outcome of the salvage procedure must be weighed against the results that might be expected after an amputation for a tumor in the same location. For tumors in the most distal part of the leg, the function, durability, and cosmetic results after treatment by amputation and prosthetic fitting are quite good.57 Small, low grade tumors can be successfully treated with limb salvage. For high grade tumors, limb salvage might be technically possible and seem like a tempting prospect, but the results are often inferior to amputation.
Functional and Psychological Outcomes
The functional outcome of the limb salvage is related to the extent of the resection, as well as the technique of the reconstruction. Detailed functional comparisons of different techniques of limb salvage are rare. 58 Several authors have 5 9—61 compared functional outcomes of limb salvage and amputation. Patients with amputations are more active and are the least worried about limb injury, but have the most impaired ambulation. Those with an arthrodesis of the knee perform the most demanding physical and recreational activities, but have difficulty sitting. Limb salvage patients have higher overall functional scores • 62 Both patients with amputations and patients who have limb salvage report a mild diminution in quality of life. Studies have failed to show a consistently significant difference between the two groups.60’63 Amputees may be more prone to feel unattractive, report difficulties finding a partner or developing sexual relationships, are embarrassed by their prosthesis, and restrict their social activities to some degree. 9,59,62
Conclusion
In the past twenty years, limb salvage has become the accepted standard of care for patients with sarcomas of the extremities. Many patients who once would have had an amputation are now having their limb saved. The success of limb salvage depends on prompt detection and early referral by the primary care doctor, and on a coordinated and carefully thought out sequence of staging, preoperative treatment, limb salvage surgery, and post—salvage support and follow-up by a dedicated team of care givers.
The goals of limb salvage are the complete eradication of the tumor with minimal complications while maintaining acceptable function, durability, and cosmesis of the limb. The limb salvage surgeon must consider the barriers to limb salvage that may exist in each particular case. Achieving a surgical margin that will ensure a low rate of local recurrence is paramount. The selection of the surgical technique for reconstruction depends on the wishes of the patient, the location of the tumor, and the extent of the surgical defect created by the resection. A variety of techniques are available so that the procedure most suitable for a particular situation can be selected. In certain cases and especially in tumors in the distal lower extremity, treatment by amputation may be preferable to limb salvage. Both limb salvage and amputation result in mild physical and psychological disabilities. Patients adapt and adjust best if they are fully informed and able to participate in the decision making process.

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Figure Legends
Figure 1. “Limb Salvage Lines” for Biopsy Placement.
If possible, the biopsy site should be located along limb salvage lines. The entire biopsy track can then be excised with the tumor at the time of definitive surgery.
Figure 2. staging System for Extremity Sarcomas. A diagram of the tumor staging system of the Musculoskeletal Tumor Society. Histologic grade is determined from biopsy material. Local extent of the tumor is determined by imaging studies. Grade and local extent are combined to determine the stage of a tumor.
Figure 3. surgical Margins in Limb Salvage Surgery. Surgical margins are defined as intralesional, marginal, wide, and radical. Intralesional margins are created when the surgical dissection enters the tumor. Marginal margins are created when the surgical dissection enters the abnormal tissue in the reactive zone around the tumor. Wide margins are created when the dissection is entirely outside the reactive zone and a cuff of normal tissue is left on all portions of the tumor. Radical margins are created by resection of all of the bony or myofascial compartments that contain the tumor.
Figure 4. Limb Salvage Surgery Resection Levels for Different Tumor Locations.
The surgeon must adjust the resection level to achieve a wide margin. When the joint is not contaminated by the tumor, intra—articular resections can be performed. When the joint is contaminated by tumor, extra—articular resection is required. When the tumors are limited to the diaphyseal or metadiaphyseal portion of a bone, intercalary resections can yield a wide margin while both adjacent joints are spared.
Figure 5. Surgical View of a Limb Salvage Reconstruction with a Megaprosthesis.
A megaprosthesis is a metallic implant designed to replace the excised bone segment along with the adjacent joints. Modular designs allow for the intraoperative customization of the protheses to suit many types of tumor resection.
Figure 6. Surgical View of a Limb Salvage Reconstruction with an osteoarticular Allograft
A size—matched osteoarticular allograft is fixed to host bone with a plate. The capsule and ligaments of the allograft are sutured to their counterparts in the host, and major muscle tendons can be sutured to their anatomic sites of insertion on the allograft. The allograft retains structurally normal articular cartilage on its joint surface.
Figure 7. Diagrammatic View of an Alloprosthetic Composite An appropriate size-matched allograft is selected to replace the resected bone segment. The articular surface of the allograft is replaced with a cemented total joint prothesis. The allograft provides bone stock and tendon insertion sites; the prosthesis provides stable, reliable joint function.
Figure 8. Diagrammatic View of a Shoulder Alloarthrodesis. The left hand figure shows the resection levels required when a tumor of the proximal humerus has contaminated the joint. The right hand figure shows an alloarthrodesis. An appropriate allograft is used to replace the resected bone. The articular surfaces are removed and the joint is immobilized with a plate while fusion occurs.

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