The Journal of Bone and Joint Surgery (American) 78:1872-88 (1996)
© 1996 The Journal of Bone and Joint Surgery, Inc.
Limb Salvage for Neoplasms of the Shoulder Girdle. Intermediate Reconstructive and Functional Results*
MARY I. O'CONNOR, M.D. , JACKSONVILLE, FLORIDA,
FRANKLIN H. SIM, M.D. and
EDMUND Y. S. CHAO, PH.D. , ROCHESTER, MINNESOTA
Investigation performed at the Department of Orthopedic Surgery, Mayo Clinic Jacksonville, Jacksonville, and the Department of Orthopedics, Mayo Clinic and Mayo Foundation, Rochester
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Abstract
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The intermediate functional results were assessed for fifty-seven patients who had had a limb-salvage procedure for treatment of a tumor of the shoulder girdle region at our institution from 1980 through 1990. Fifty-three patients had a malignant bone tumor (a sarcoma) and four had an extensive giant-cell tumor. The resections were classified according to the system of the Musculoskeletal Tumor Society. A variety of reconstructive procedures were performed after resection of the tumor, with the choice of procedure depending on the type of resection and the needs of the patient. The functional results were described and graded quantitatively according to the functional rating system of the Musculoskeletal Tumor Society.
The average duration of follow-up was 5.3 years (median, 4.6 years) for the forty-seven patients who were still alive at the time of the latest follow-up examination. Eight patients died of disease and two others died of unrelated malignant tumors an average of 1.8 years postoperatively. The resection of the tumor was classified as wide in forty of the fifty-three patients who had a sarcoma and as marginal in thirteen; four patients had local recurrence (two, after a wide resection, and two, after a marginal resection). One of the four patients who had a giant-cell tumor had local recurrence.
The functional results were related to the type of resection and the method of skeletal reconstruction. After resection of the entire scapula and the proximal aspect of the humerus, reconstruction with a spacer frequently resulted in asymptomatic superior subluxation of the implant and poor function of the shoulder. After extra-articular resection of the glenoid cavity and the proximal aspect of the humerus with loss of the abductor mechanism, osseous arthrodesis resulted in good function that was superior to that found after reconstruction with a spacer or a proximal humeral replacement prosthesis. Our preferred method to achieve fusion was insertion of an intercalary allograft and a vascularized fibular graft. However, the allograft fractured in three of four patients in whom primary fusion had been obtained with this technique. An osteoarticular allograft inserted after intra-articular resection of the proximal aspect of the humerus and preservation of the abductor mechanism provided good function that was superior to that found after reconstruction with a proximal humeral replacement prosthesis, which produced symptomatic instability that led to a secondary arthrodesis in some patients. However, subchondral fracture and collapse of the osteoarticular allograft occurred in four of eight patients by the time of the latest follow-up examination.
The results of all methods of reconstruction were satisfactory with regard to pain, emotional acceptance, and manual dexterity. We believe that the use of a method of reconstruction that is appropriate with regard to the needs of the patient and preoperative counseling regarding the expected functional level and restrictions of activity are critical for a high level of postoperative satisfaction.
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Introduction
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Curative resections that spare the limb are often possible in patients who have a malignant tumor or a destructive benign tumor of the shoulder girdle. Reconstruction after these limb-sparing resections, however, remains a problem. Because none of the prosthetic devices that are currently available compensate adequately for the functional deficits after amputation, continued efforts to improve reconstructive methods are warranted.
The purpose of this study was to review the intermediate results of various reconstructive procedures that had been performed after resections of neoplasms of the shoulder girdle. The emphasis was on the relationship of the type of resection and reconstructive procedure with the functional result.
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Materials and Methods
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Clinical Series
Fifty-seven patients had a non-ablative operation at our institution for treatment of a primary sarcoma of bone or an extensive benign giant-cell tumor of the shoulder girdle from January 1980 through May 1990. Thirty-two patients were male, and twenty-five were female. The average age was thirty-five years (range, five to seventy-one years). The study included only patients who had a bone neoplasm of the scapula or the proximal aspect of the humerus; patients who had a soft-tissue sarcoma or bone tumor of the clavicle or the proximal part of the humeral diaphysis (without involvement of the humeral head) were excluded. Patients were selected for a limb-sparing resection when the preoperative imaging studies suggested that a satisfactory surgical margin could be achieved and, if metastatic disease were present, that the metastatic disease also appeared amenable to resection. All patients who met these criteria during the time-interval of this study were included.
The skeletal resections were classified according to the system of the Musculoskeletal Tumor Society12 (Fig. 1), which is a modification of the classification scheme proposed by Malawer22. The functional results were described and graded quantitatively according to the most recent functional rating system of the Musculoskeletal Tumor Society13 (Table I).

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Fig. 1 Illustration of the Musculoskeletal Tumor Society classification
of skeletal resections about the shoulder girdle12. At least one-half of the region must be
resected to be so designated. S1 = the blade or spine of the scapula, S2 =
the acromion-glenoid cavity complex (the glenoid cavity must be removed),
S3 = the proximal epiphysis of the humerus, S4 = the proximal metaphysis of
the humerus, and S5 = the proximal part of the diaphysis of the humerus.
(With permission of the Mayo Foundation.)
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The average duration of follow-up was 4.6 years. Ten patients died an average of 1.8 years postoperatively (range, 0.25 to 7.3 years). The average duration of follow-up for the forty-seven surviving patients was 5.3 years (median, 4.6 years; range, 2.0 to 11.6 years). The most recent examination was performed by a physician at our institution for twenty-seven of the forty-seven patients and by a local physician for five others. Follow-up data on the remaining fifteen patients were obtained with use of a written questionnaire.
Seventeen of the tumors were of the scapula and forty were of the proximal aspect of the humerus (Fig. 2). There were twenty-four chondrosarcomas, twenty-two osteosarcomas, six Ewing sarcomas, one fibrosarcoma, and four giant-cell tumors (Table II). The surgical stage11 was IA for three of the twenty-four chondrosarcomas, IB for seven, IIA for one, and IIB for thirteen. Two of the osteosarcomas were stage IB, one was stage IIA, fifteen were stage IIB, and four were stage III. All of the Ewing sarcomas and the fibrosarcoma were stage IIB (Table II). The osteosarcomas and chondrosarcomas accounted for nearly 87 per cent of the malignant tumors. Of the four patients who had a stage-III osteosarcoma, two had pulmonary metastases, one had a single metastasis to bone, and one had both bone and pulmonary metastases; all of the metastatic lesions were believed to be resectable. All four of the giant-cell tumors were benign stage-III lesions9.

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Fig. 2 Illustration showing the location of the neoplasms in the
fifty-seven patients who were managed with a limb-sparing resection. Of the
seventeen lesions in the scapula, eight involved both region S1 and region
S2. Of the forty tumors in the proximal aspect of the humerus, four
extended from region S4 into region S5 (the metaphysis into the diaphysis),
seven involved regions S3, S4, and S5 (the entire proximal aspect of the
humerus), three involved only region S4, twenty-five involved both region
S3 and region S4 (the epiphysis and metaphysis), and one involved only
region S3. (With permission of the Mayo Foundation.)
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Symptoms at presentation included pain in fifty-four patients and a pathological fracture in eleven. On physical examination, a palpable mass was noted in thirty-two patients and an axillary nerve palsy, in one. Eight patients had recurrent sarcoma at presentation. Preoperative staging studies included plain radiographs of the shoulder, magnetic resonance imaging or computed tomography images of the region around the tumor, a total-body technetium bone scan, and computed tomography images of the chest.
Forty-seven patients had an open biopsy and ten had a core needle biopsy. Twenty-seven patients had the initial biopsy performed at another institution, and the biopsy was believed to have had a potentially negative effect on the subsequent treatment of eight of them. Poor placement of the site of the biopsy necessitated alteration of the operative approach in five patients, and three patients had contamination of tissue.
The administration of chemotherapy was not uniform, given the time-span of this study. Of the twenty-two patients who had an osteosarcoma, seven received chemotherapy both preoperatively and postoperatively; ten received it only preoperatively; and five did not receive chemotherapy because of low-grade disease (two patients), treatment very early in the series (two patients), or advanced age (one patient). Two patients who had a dedifferentiated chondrosarcoma and the patient who had fibrosarcoma received chemotherapy preoperatively. Of the six patients who had a Ewing sarcoma, four received chemotherapy both preoperatively and postoperatively and two received it only postoperatively.
Adjuvant external-beam radiation therapy was administered to three patients, all of whom had a Ewing sarcoma. One patient received 4480 centigray preoperatively and 1680 centigray postoperatively, one received 5028 centigray postoperatively, and one received an unspecified dose postoperatively.
Oncological and Reconstructive Procedures
The surgical margin9 was wide in thirty-nine of the fifty-three patients who had sarcoma, contaminated wide in one, marginal in eleven, and contaminated marginal in two. The giant-cell tumors were treated with marginal excision in two patients and with intralesional excision in the other two.
The extent of the resection was classified according to the system of the Musculoskeletal Tumor Society12. With this system, the shoulder girdle is divided into five sections (Fig. 1) and the status of the abductor mechanism (the deltoid and the muscles of the rotator cuff) is denoted by an A if it is "intact," which indicates that it is available for reconstruction, or by a B if it is "disrupted," which indicates that reconstruction of these functional units is not possible. The status of the abductor mechanism is an important factor in the determination of the method of reconstruction. For example, after resection of the proximal humeral epiphysis and metaphysis, reconstruction with an osteoarticular allograft is considered if the abductor mechanism is intact, whereas arthrodesis is considered if it is disrupted.
The resections performed in this study included resection of the scapular blade with the abductor mechanism intact (S1A), resection of the glenoid cavity with the abductor mechanism disrupted (S2B), resection of the entire scapula with the abductor mechanism disrupted (S12B); resection of the entire scapula and the proximal humeral epiphysis and metaphysis with the abductor mechanism disrupted (S1234B); resection of the glenoid cavity and proximal humeral epiphysis and metaphysis with the abductor mechanism disrupted (S234B); resection of the glenoid cavity and the proximal humeral epiphysis, metaphysis, and diaphysis with the abductor mechanism disrupted (S2345B) (Figs. 3-A, 3-B, 4-A, 4-B, 4-C, 4-D, 4-E, 4-F, 5-A, 5-B, 5-C, 5-D through 5-E); resection of the proximal humeral epiphysis and metaphysis with the abductor mechanism intact (S34A) or disrupted (S34B) (Figs. 6-A, 6-B, 6-C, 6-D, 7-A through 7-B), and resection of the proximal humeral epiphysis, metaphysis, and diaphysis with the abductor mechanism intact (S345A) or disrupted (S345B).

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Figs. 3-A and 3-B: Anteroposterior radiographs of a thirty-two-year-old man who had stage-IIB fibroblastic osteosarcoma of the proximal aspect of the humerus.
Fig. 3-A: Radiograph made at presentation. Chemotherapy with mitomycin, Adriamycin (doxorubicin), and cisplatin was administered preoperatively.
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Fig. 3-B: Radiograph made five years after an extra-articular S2345B resection and reconstruction with a modular metal spacer sutured to the remaining scapula and cemented into the humeral canal. The lateral aspect of the clavicle was also resected, and chemotherapy was administered postoperatively. There was osteopenia and slight stress-shielding of the remaining distal aspect of the humerus. The implant was stable. At the time of follow-up, the patient had been continuously free of disease and had no pain in the shoulder. He was enthusiastic about the result, and he stated that he had only recreational restrictions. Active positioning of the hand and lifting ability were rated as poor, and the over-all functional rating was 67 per cent.
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Figs. 4-A through 4-F: A thirteen-year-old girl who had stage-IIB osteosarcoma of the proximal aspect of the humerus.
Fig. 4-A: Anteroposterior radiograph made after neoadjuvant chemotherapy.
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Fig. 4-B Anteroposterior radiograph made five months after an extra-articular S2345B wide resection and reconstruction with an arthrodesis with an intercalary allograft and a vascularized fibular graft. A latissimus dorsi flap was used for soft-tissue coverage. Chemotherapy had been administered postoperatively. The site of the allograft and humeral osteotomy was visible distally; good union was evident in all other regions. Subsequent radiographs demonstrated distal union as well by twenty-two months postoperatively.
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Fig. 4-C Illustration of the technique of arthrodesis with intercalary
allograft and vascularized fibular graft in shoulder-limb salvage. (With
permission of the Mayo Foundation.)
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Figs. 4-D and 4-E: Photographs made eighteen months postoperatively. The patient had 90 degrees of active forward flexion. The functional rating was excellent with regard to stability and emotional acceptance and was good with regard to the remaining categories. The over-all functional rating was 77 per cent.
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Figs. 4-D and 4-E: Photographs made eighteen months postoperatively. The patient had 90 degrees of active forward flexion. The functional rating was excellent with regard to stability and emotional acceptance and was good with regard to the remaining categories. The over-all functional rating was 77 per cent.
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Fig. 4-F Anteroposterior radiograph made at the latest follow-up evaluation, 3.5 years after the resection. The patient had remained continuously free of disease. Of note, the patient fell two years after the operation and sustained a longitudinal stress fracture through the allograft in the region without plate fixation. A shoulder-spice cast was applied and worn for three months, with subsequent clinical union and radiographic hypertrophy of the vascularized fibular graft and increased osseous density in the region of the fractured allograft.
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Figs. 5-A through 5-E: Anteroposterior radiographs of a thirteen-year-old boy who had stage-IIB chondroblastic osteosarcoma of the proximal aspect of the humerus.
Fig. 5-A: Radiograph made after one month of preoperative chemotherapy.
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Fig. 5-B Radiograph made after an S2345B wide resection followed by press-fitting of a temporary spacer into the humeral canal.
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Fig. 5-C: Radiograph made nearly two years after removal of the temporary spacer and the planned insertion of an implant to achieve prosthetic fusion. There is gross loosening of the press-fit stem necessitating revision.
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Fig. 5-D: Radiograph made after revision with a new custom ingrowth component with distal fixation with cement.
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Fig. 5-E: Radiograph made two and a half years after the revision, showing marked lucency at the bone-cement interface. Despite this gross loosening, the patient did not have any pain. The over-all functional rating was 47 per cent because of poor ratings for function, positioning of the hand, and lifting ability.
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Figs. 6-A through 6-D: Anteroposterior radiographs of a nineteen-year-old woman who had a benign stage-III giant-cell tumor9 of the proximal aspect of the humerus.
Fig. 6-A: Radiograph made at presentation.
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Fig. 6-B Radiograph made five months after an S34A resection and reconstruction with an osteoarticular allograft.
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Fig. 6-C: Radiograph made twenty-six months postoperatively. The articular surface of the graft collapsed. Lucency in the region of the greater tuberosity had been noted previously and the allograft was thought to be stable. The functional rating, which had been good one year postoperatively, was now fair.
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Fig. 6-D: Radiograph made after revision to an allograft-prosthetic composite by insertion of a long-stem humeral endoprosthesis with cement. Recurrence of the giant-cell tumor was found in the lucent region of the greater tuberosity of the allograft and was treated with curettage, application of phenol, and cementation.
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Figs. 7-A and 7-B: Anteroposterior radiographs of a forty-eight-year-old-woman who had a stage-IA chondrosarcoma of the proximal aspect of the humerus that was treated with an S34A wide resection and reconstruction with a proximal humeral replacement prosthesis. The tendons of the rotator cuff were sutured to the prosthesis.
Fig. 7-A: Radiograph made ten months postoperatively. The patient had symptomatic instability.
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Fig. 7-B Radiograph made 4.5 years after a secondary arthrodesis with vascularized and non-vascularized fibular grafts. The fusion was solid, with excellent hypertrophy of the fibular grafts. The over-all functional rating was 63 per cent, with a satisfactory rating with regard to all factors except positioning of the hand, which was limited to that possible with 70 degrees of forward flexion of the shoulder.
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The method of reconstruction varied according to the extent of the resection.
Scapular Lesions
Reconstruction was not necessary for the five patients who had an S1A resection. A primary arthrodesis was performed in the patient who had an S2B resection. An attempt was made to stabilize the humeral head beneath the clavicle in the four patients who had an S12B resection. Six of the seven patients who had a classic Tikhoff-Linberg procedure19 (an S1234B resection) had reconstruction with a modular metal spacer cemented distally into the humeral canal and sutured proximally to the chest wall14; the remaining patient did not have reconstruction (Table III).
Proximal Humeral Lesions
A reconstructive procedure was performed in all forty patients who had a lesion of the proximal aspect of the humerus (Table III). Twelve patients had an S34A resection. Four of them had reconstruction with a proximal humeral replacement prosthesis early in the series, seven had an osteoarticular allograft, and one (a young rancher who placed very high demands on the upper extremities) had a primary arthrodesis with use of an intercalary allograft and a vascularized fibular graft.
Nine patients had an S34B or S345B resection. Seven patients had reconstruction with a proximal humeral replacement prosthesis; one patient, who had pulmonary metastases, had insertion of a modular spacer; and one patient, in whom the axillary nerve had been resected but the rotator cuff had been preserved, had an osteoarticular allograft.
Extension of the tumor into the glenohumeral joint necessitated an S234B or S2345B resection in nineteen patients. A modular spacer was used for reconstruction in seven patients (Figs. 3-A and 3-B). Four patients had implantation of a proximal humeral replacement prosthesis that functioned as a spacer rather than as an endoprosthesis because the glenoid cavity had been resected; thus, it was considered to be a spacer for the purpose of analysis.
An arthrodesis was performed as a primary or delayed reconstruction in the remaining eight patients. Four patients had a primary arthrodesis with an intercalary allograft and a vascularized fibular graft (Figs. 4-A, 4-B, 4-C, 4-D, 4-E through 4-F). The vascularized fibular graft was used as an adjunct in an attempt to promote early osseous union. In four patients, a temporary press-fit spacer was inserted at the time of the excision of the tumor. The decision to implant a temporary prosthesis was influenced by the administration of postoperative chemotherapy, the need for a thoracotomy for resection of pulmonary metastases, or an extremely young age. Two patients had a planned removal of the temporary prosthesis and insertion of a permanent implant in an attempt to achieve a prosthetic fusion (an implant bridging the defect from the scapula to the humeral shaft) at ten months (Figs. 5-A, 5-B, 5-C, 5-D through 5-E) and fifteen months after resection of the tumor. The other two patients had a good result with the temporary implant until four and five years after excision of the tumor, at which time a prosthetic implant to achieve fusion was inserted in one patient and an osseous arthrodesis was performed with a vascularized fibular graft in the other.
All patients who had an arthrodesis and eight patients who had reconstruction with a spacer wore a shoulder-spice cast, for an average of fourteen and eight weeks, respectively. A shoulder immobilizer was used in the immediate postoperative period for the remaining patients.
Techniques of Arthrodesis
The techniques of internal fixation of the site of the arthrodesis varied according to the procedure. Fixation with a plate and screw was used for the primary arthrodeses, and internal stabilization with several screws was employed for the arthrodesis with a single vascularized fibular graft.
Two plates and multiple screws were used for the arthrodeses with an intercalary allograft and a vascularized fibular graft (Fig. 4-B). Our technique was similar to that described by Richards and Kostuik28. The intercalary allograft was fashioned from an osteoarticular proximal humeral allograft. Osteotomy of the epiphyseal region of the allograft was performed to maximize osseous contact with the remaining glenoid cavity. Cancellous-bone screws were placed across the allograft and into the glenoid cavity. A dynamic compression plate was contoured and fixed to lie along the scapular spine, the acromion, and the lateral aspect of the allograft.
In some patients, an attempt was also made to obtain fusion across the acromion-allograft region through good contact of the allograft with the decorticated undersurface of the acromion. A second plate was applied at the distal allograft-host bone junction. The vascularized fibular graft was then placed anteriorly by one of our colleagues, who is experienced with this technique17, and was typically secured to the proximal and distal regions of the host bone with one or two screws. The position of the shoulder for the arthrodesis was generally 30 degrees of abduction from the side of the body, 30 degrees of forward flexion, and 20 to 30 degrees of internal rotation. Care was taken to ensure that the hand could readily reach the mouth and that excessive winging of the scapula was not noted with the arm at the side of the body.
Soft-Tissue Reconstruction
The method of soft-tissue reconstruction depended on the extent of the bone and soft-tissue resection. In patients who had an intra-articular resection and an intact abductor mechanism (an S34A resection), the tendons of the rotator cuff were sutured to the allograft tendon or as a sleeve of soft tissue around the proximal humeral replacement prosthesis. In patients who had an intra-articular resection and disruption of the abductor mechanism (an S34B or S345B resection), all or part of the static and dynamic suspension technique described by Malawer et al.24 was used for reconstruction with a proximal humeral replacement prosthesis.
The technique described by Malawer et al.24 was also used after an extra-articular resection with disruption of the abductor mechanism (an S234B or S2345B resection) in four patients who had reconstruction with a proximal humeral replacement prosthesis that functioned as a spacer. For twelve other patients, including five of the eight who had a primary or delayed arthrodesis, rotational latissimus dorsi flaps were needed for adequate soft-tissue coverage of the reconstruction. Care must be taken during resection of a tumor of the shoulder girdle or a thoracotomy not to disrupt the blood supply to the latissimus dorsi.
Because of extensive soft-tissue resection, three of the six patients who had a classic Tikhoff-Linberg resection19 and reconstruction with a modular spacer needed a rotational latissimus dorsi flap (two patients) or a rotational pectoralis major flap (one patient) for adequate coverage of the spacer. Although the spacer is not bulky, adequate soft-tissue coverage is still necessary.
Functional Rating System
The system adopted by the Musculoskeletal Tumor Society and the International Symposium on Limb Salvage for the evaluation of function following reconstructive procedures after operative treatment of musculoskeletal tumors13 (Table I) was used in this study.
Functional data were available for forty-two of the fifty-seven patients. Forty-one of the forty-two patients were alive at the time of the most recent follow-up, and one had died of an unrelated malignant tumor several years postoperatively. Of the other fifteen patients, eight had died of disease, one had died of an unrelated malignant tumor, two had had a recent revision operation, three had insufficient functional data for assessment, and one had a complication related to the reconstructive procedure that prohibited functional assessment. The follow-up period, which was either from the most recent reconstructive procedure or from treatment of a complication related to the reconstructive procedure to the time of the functional assessment, averaged 4.4 years (median, 4.2 years; range, 1.8 to 10.0 years).
The functional evaluation was performed by both a physician and an assistant from the Biomechanics Laboratory at our institution for seventeen patients, by a physician at our institution for eight patients, by a local physician (one of whom was an orthopaedic oncologist) for three patients, and with use of a written questionnaire for fourteen patients. Patients who completed the questionnaire were asked to rate pain, functional activity, emotional acceptance, positioning of the hand, manual dexterity, and lifting ability (Table I). The questionnaire included drawings of the shoulder in flexion and abduction that enabled patients to indicate their active motion, in order to determine the appropriate rating for positioning of the hand.
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Results
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Oncological Evaluation
Forty-three (81 per cent) of the fifty-three patients who had a sarcoma and all four of the patients who had a giant-cell tumor were alive with no evidence of disease at an average of 5.3 years (median, 4.6 years) postoperatively. Eight (15 per cent) of the patients who had a sarcoma died of the disease, an average of 1.8 years postoperatively, and two died of unrelated malignant tumors.
Of the twenty-four patients who had a chondrosarcoma, twenty-one (88 per cent) had no evidence of disease at the time of the most recent follow-up. Pulmonary metastases developed in three patients; one was managed successfully with a thoracotomy and the other two patients died. Another patient died of an unrelated malignant tumor. Two patients (8 per cent) had local recurrence, which was treated with wide excision in one and with marginal excision in the other. One patient remained disease-free after the excision of the recurrent tumor, and the other had another recurrence, which was treated with forequarter amputation; this patient is one of the two who subsequently died of pulmonary metastases.
Of the twenty-two patients who had an osteosarcoma, nineteen (86 per cent) remained disease-free, including two of the four patients who had had metastatic disease at presentation that was treated with a thoracotomy (one patient) or resection of bone (one patient). Three patients, including the remaining two patients who had had metastatic disease at presentation, died of metastatic disease before the latest follow-up examination. Local recurrence along the axillary vessels developed in one patient who had initially had resection with a wide margin. A forequarter amputation was performed, but the patient subsequently died of pulmonary metastases.
Three of the six patients who had a Ewing sarcoma were alive at the time of the latest follow-up. Pulmonary and skeletal metastases had developed in the other three patients. One of these patients also had had local recurrence after a contaminated marginal excision.
The patient who had a fibrosarcoma of bone died of an unrelated malignant tumor.
One of the four patients who had a giant-cell tumor had local recurrence (Figs. 6-A, 6-B, 6-C through 6-D). The case of this patient is particularly noteworthy because the recurrence was within the allograft.
All five patients who had local recurrence had had a biopsy before referral to our institution, and poor biopsy technique was documented for one. Recurrence was detected an average of eight months after the resection. The surgical stage11 had been IIB in all four patients who had local recurrence of a sarcoma.
Results of the Reconstructive Procedures
The results of the reconstructive procedures, the functional outcomes, and any complications were analyzed according to the type of resection and the method of reconstruction (Table IV).
Functional Spacer
Reconstruction with a modular spacer or a proximal humeral replacement prosthesis can stabilize the limb to the chest wall after resection of the proximal aspect of the humerus and either the glenoid cavity or the entire scapula. Although little function is restored to the shoulder, such reconstructions provide a stable fulcrum for function of the elbow and hand and prevent pain related to traction on the neurovascular bundle.
The eighteen patients who had reconstruction with a functional spacer generally fared well from a reconstructive standpoint (Figs. 3-A and 3-B). Problems related to these spacers included subluxation and bone loss secondary to stress-shielding. Of the eighteen patients who had had reconstruction with a modular spacer or a proximal humeral replacement prosthesis functioning as a spacer, seven had one to four centimeters of subluxation of the implant, usually superiorly. However, only one patient had more than mild residual symptoms. Attempted restabilization of the modular spacer to the remaining scapula and the ribs in this patient was unsuccessful, and the patient refused a secondary arthrodesis or additional operative treatment.
In five patients, mild stress-shielding was noted at the prosthesis-bone junction (Figs. 3-A and 3-B). This was manifested radiographically as resorption involving no more than one-half of the circumference of the first one to two centimeters of the adjacent humerus. Loosening of the cemented stem of the modular spacer within the humeral canal was not seen. One patient who had a proximal humeral replacement prosthesis had radiographic evidence of loosening but had no major symptoms at the time of the most recent follow-up examination.
Functional data were available for eleven of the eighteen patients. The average over-all functional rating was 49 per cent for five patients after an S1234B resection (Table IV) and 54 per cent for six patients after an S234B or S2345B resection (Figs. 3-A and 3-B). On the average, the results with the functional spacers were rated as satisfactory (a score of 3.0 points or more) with regard to pain, emotional acceptance, and manual dexterity and as unsatisfactory (a score of less than 3.0 points) for function, positioning of the hand, and lifting ability (Table V).
Complications associated with this reconstruction included a brachial plexopathy that resolved with time but necessitated later release of residual metacarpophalangeal contractures. Another patient had delayed wound-healing that did not necessitate treatment.
Proximal Humeral Replacement Prosthesis
Of the eleven patients who had reconstruction with a proximal humeral replacement prosthesis after an S34 or S345 resection, two subsequently had mild stress-shielding at the humerus-prosthesis junction, six had subluxation of the prosthesis, one had a deep infection that led to débridement without removal of the implant, and two had loosening or fracture of a ceramic prosthesis.
A secondary arthrodesis was performed ten months and four years postoperatively in two patients who had symptomatic instability and twenty-two months and four years postoperatively in the two patients who had failure of a ceramic prosthesis. The arthrodesis was performed with an intercalary allograft and a vascularized fibular graft in three patients and with vascularized and non-vascularized fibular grafts in one. The arthrodesis performed with vascularized and non-vascularized fibular grafts (Figs. 7-A and 7-B) and one of those performed with an intercalary allograft and a vascularized fibular graft were followed by healing without complications.
Functional data were available for six of the seven patients who did not have a secondary arthrodesis. The over-all functional rating was 66 per cent for four patients after a S34A resection and 52 per cent for two patients after a S34B or S345B resection. On the average, the results with the proximal humeral replacement prostheses were satisfactory with regard to pain, emotional acceptance, and manual dexterity and unsatisfactory with regard to function, positioning of the hand, and lifting ability.
Complications included thrombosis of the brachial artery and compartment syndrome of the forearm in one patient who had had a secondary arthrodesis with an intercalary allograft and a vascularized fibular graft. These were treated successfully with thrombectomy and fasciotomy. Deep infection subsequently developed, necessitating removal of the allograft. A second vascularized fibular graft was placed to achieve fusion. The vascularized fibular graft remained viable and was retained. Subsequent fracture of both fibulae led to internal fixation and solid union was again achieved.
Deep infection also developed in another patient who had a secondary arthrodesis with an intercalary allograft and a vascularized fibular graft. The allograft was removed and the vascularized fibular graft was retained, with subsequent distal union and a stable proximal pseudarthrosis.
Arthrodesis
Allogenic or autogenous graft techniques were used in seven of the ten patients who had reconstruction with an immediate or staged primary arthrodesis and an implant was used to achieve fusion in three. Six of the seven primary or staged osseous procedures were successful. These included the primary glenohumeral arthrodesis (after an S2B resection), the staged arthrodesis performed with a single vascularized fibular graft, and four of the five primary arthrodeses performed with an intercalary allograft and a vascularized fibular graft (Figs. 4-A, 4-B, 4-C, 4-D through 4-E). The one failure was due to deep infection that led to removal of the allograft, and a subsequent salvage arthrodesis with a second vascularized fibular graft was successful.
Of the four patients who had a successful primary arthrodesis with an intercalary allograft and a vascularized fibular graft, two sustained a stress fracture of the allograft at seven and twenty-five months after the arthrodesis (Fig. 4-F). These patients were managed with immobilization in a shoulder-spica cast for approximately three months, and the fractures healed from a clinical standpoint, with radiographic hypertrophy of the intact adjacent vascularized fibular graft. One patient sustained a fracture of the intercalary allograft and the vascularized fibular graft thirty-one months after the arthrodesis. Internal fixation was recommended but declined, and the patient had an asymptomatic pseudarthrosis at the latest follow-up examination. Overlapping dynamic compression plates were used in two of the three patients who had a fracture.
Functional scores were available for ten of the eleven patients who had an osseous arthrodesis: five who had a primary arthrodesis, four who had a secondary arthrodesis after failure of a proximal humeral replacement prosthesis or an infection at the site of an arthrodesis with an intercalary allograft or a vascularized fibular graft, and one who had a pseudarthrosis after a secondary arthrodesis. The average over-all functional rating was 79 per cent after primary arthrodesis, 60 per cent after secondary arthrodesis, and 50 per cent for the patient who had a pseudarthrosis. The results of the arthrodeses were rated as satisfactory with regard to pain, function, emotional acceptance, and manual dexterity and unsatisfactory with regard to positioning of the hand. Lifting ability was satisfactory after the primary arthrodeses but unsatisfactory after the secondary arthrodeses.
Complications encountered with this procedure included impingement on the brachial artery, due to local pressure from a latissimus dorsi flap, in one patient. This was treated successfully with loosening of the flap. Three patients had complications related to the donor site of the vascularized fibular graft, including a suspected compartment syndrome (which was treated with a fasciotomy), temporary peroneal nerve palsy, and contracture of the long flexor tendon of the great toe17.
Of the three patients who had insertion of an implant to achieve prosthetic fusion, one had a satisfactory result, with a solid union at the distal prosthesis-humerus junction and a stable fibrous union at the prosthesis-scapula interface. One patient had revision of a loose press-fit humeral component to one inserted with cement two years after the initial procedure. Screws were used for proximal fixation of the prosthesis in both the primary and the revision procedure. Despite recurrent distal loosening, the patient had minor symptoms three years later (Figs. 5-A, 5-B, 5-C, 5-D through 5-E). Fourteen months postoperatively, the remaining patient noted rotational instability between modular fiber-metal components that had been used to provide the option of subsequent lengthening. Despite replacement of the set screws of the modular components, additional junctional bone-grafting, and immobilization in a shoulder-spica cast for three months, mild asymptomatic rotational instability persisted at the time of the latest follow-up evaluation at four years.
The average over-all functional rating for the three patients who had insertion of an implant to achieve prosthetic fusion was 61 per cent, with satisfactory ratings for pain, emotional acceptance, and manual dexterity. Function, positioning of the hand, and lifting ability were rated as unsatisfactory.
Osteoarticular Allograft
All eight patients who had had reconstruction with an osteoarticular allograft had osseous union at the allograft-humerus junction. However, the articular and subchondral region of the allograft had fractured and collapsed in four of these patients by the latest follow-up evaluation. Three of the patients were asymptomatic or had only slight aching with increased activity. Progressive discomfort developed in the fourth patient, who had an endoprosthetic revision shortly before the latest follow-up examination, with local recurrence of a giant-cell tumor found within the allograft (Figs. 6-A, 6-B, 6-C through 6-D). One patient had a fracture between the metaphyseal and diaphyseal regions of the allograft eleven months postoperatively, and this was treated with revision to a second osteoarticular allograft at another institution. Functional data were unavailable for the latter two patients.
The over-all functional rating for the six patients for whom it was available was 71 per cent (Table IV). On the average, the results were rated as satisfactory in all categories except function and positioning of the hand. The three patients who had articular collapse and for whom a functional rating was available tended to have slightly lower scores for pain, emotional acceptance, and positioning of the hand, compared with the three patients who did not have collapse of the allograft.
No Reconstruction
Osseous reconstruction was not performed after the S1A or S12B resections. The average over-all functional rating for the three patients who had an S1A resection and for whom a rating was available was 77 per cent (Table IV), and the average result was satisfactory for all factors. The average over-all functional score for the two patients who had an S12B resection and for whom a rating was available was 45 per cent, with a satisfactory result with regard to only pain and manual dexterity. The over-all functional score for the patient with a Tikhoff-Linberg resection19 (an S1234B resection) and no reconstruction was 43 per cent, with satisfactory results with regard to pain, emotional acceptance, and manual dexterity.
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Discussion
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Salvage of the limb for patients who have a malignant or destructive benign neoplasm of the shoulder girdle continues to pose challenges from both an oncological and a reconstructive standpoint. Although advances in imaging techniques (principally magnetic resonance imaging) permit more accurate definition of the extent of the tumors and more precise operative planning, recurrence continues to be a problem.
Five (9 per cent) of the fifty-seven patients in the current series had local recurrence. Other authors have reported rates of 0 per cent23,31 to 15 per cent2. In four substantial series2,16,23,32, with a total of 157 patients and an average duration of follow-up of five years, we calculated a cumulative rate of local recurrence of 10 per cent.
All five of the patients who had local recurrence in our series had had a biopsy before referral to our institution. An increased prevalence of complications related to biopsy performed before referral to the treating institution was well documented by Mankin et al.25 more than ten years ago and again recently. Other studies have also shown this trend34. We continue to support the recommendation put forth by Mankin et al. that the biopsy be performed by the surgeon who will subsequently provide the definitive operative treatment.
Of particular interest in the present series was the patient who had a recurrent giant-cell tumor within the greater tuberosity of the osteoarticular allograft. Whereas local recurrence of a giant-cell tumor within soft tissue has been reported20,27,30, we are not aware of a reported recurrence within an allograft. We speculate that residual tumor remained in the tendon of the rotator cuff at the time of the resection, with subsequent seeding of the allograft.
The choice of reconstruction should be based on the extent of the resection and the needs of the patient (Table VI). The results regarding certain functional factors depend on the type of reconstruction used. With regard to positioning of the hand and lifting ability, the functional results after reconstructions with an osseous arthrodesis or an osteoarticular allograft were better than those with a proximal humeral replacement prosthesis or a spacer. Of note, however, are the satisfactory ratings for pain and manual dexterity for all forty-two patients who had a functional evaluation. Furthermore, thirty-eight (90 per cent) of the forty-two patients rated emotional acceptance as satisfactory ("Would do again.") or better. We believe that preoperative counseling regarding the expected functional outcome is crucial to achieving a high level of postoperative emotional acceptance by the patient.
No reconstruction is needed after resection of the scapular blade, and good functional results were seen in our small group. Options after total scapulectomy (S12B resection) include no reconstruction, reconstruction with a scapular spacer6,7, and medial subclavicular displacement8. We have not performed any reconstruction routinely in this setting. Functional results were available for only two of the four patients who had complete excision of the scapula, but they suggested over-all unsatisfactory function.
Options for reconstruction after a classic Tikhoff-Linberg resection19 (an S1234B resection) include stabilization of the remaining limb with a spacer or proximal humeral replacement prosthesis as well as no reconstruction at all. The functional ratings were poor for five patients in the present series who had S1234B resection and reconstruction with a spacer. These patients typically had a poor rating for both positioning of the hand and lifting ability. Distal function was preserved. The results with regard to pain and emotional acceptance were satisfactory, and use of the spacer permitted resumption of chemotherapy without delay.
With use of the previous functional rating system of the Musculoskeletal Tumor Society10, Capanna et al.2 noted fair functional results for eight patients who had had an S1234B or S12345B resection and reconstruction with a constrained modular proximal humeral replacement prosthesis. Five of fourteen patients who had had excision of the scapula and the proximal humeral epiphysis (an S123B resection) and reconstruction with this device had good function, six had fair function, and three had poor function2.
Courpied et al.4 reported fair functional results, according to the modified functional rating system of the Musculoskeletal Tumor Society, with use of a Mathy-type proximal humeral replacement prosthesis (a massive metallic implant or a massive plastic implant with a metallic core) in three patients who had had an S123B resection. The functional result was fair in two patients and poor in five after an S1234B or S12345B resection without a reconstructive procedure.
One of the most challenging reconstructive situations in shoulder-limb salvage is that after resection of the glenoid cavity and the proximal aspect of the humerus (an S234B or S2345B resection). Reconstructive options include use of a spacer or proximal humeral replacement prosthesis, an allograft-prosthetic composite, and an arthrodesis. Reconstruction with a spacer or proximal humeral replacement prosthesis offers immediate distal fixation and the ability to administer radiation therapy in the early postoperative period. It is also generally the least time-consuming procedure of the available options. However, although arthrodesis is a more arduous procedure, it generally provides better function.
In the present series, S234B and S2345B resections with use of a functional spacer resulted in an average over-all functional rating of 54 per cent, clearly less than that after arthrodesis. Capanna et al.2 noted good function for six patients and fair function for six patients who had a constrained proximal humeral prosthesis anchored to the remaining scapula. Courpied et al.4 reported a fair functional result for two patients and a poor functional result for three patients in whom an intramedullary nail had been used as a spacer. Three of these patients subsequently had the nail removed because it was not fixed firmly and irritation of the surrounding soft tissues was painful.
In our experience, osseous arthrodesis produced functional results that were superior to those after reconstruction with a proximal humeral replacement prosthesis or spacer after an S234B or S2345B resection. Of our seven patients who had had an S234B or S2345B resection and reconstruction with a primary osseous arthrodesis or a secondary osseous arthrodesis and for whom functional results were available, six (five and one, respectively) had good function more than four years postoperatively. Enneking8 noted that "arthrodesis ... is in principle an active arthroplasty that transfers the site of motion from the glenohumeral joint to the thoracoscapular `joint'."
Gebhardt et al.15 reported their early experience with allograft arthrodesis in seven patients after six to twenty-three months of follow-up. The functional result was excellent for four patients and good for three. Peabody et al.26 noted "stable, pain-free shoulders with sufficient scapulo-thoracic and elbow motion to perform activities of daily living" in five patients nine to forty-four months after allograft arthrodesis of the shoulder. Long-term functional results of glenohumeral arthrodesis performed for non-tumor-related conditions suggest that functional results do not deteriorate with time3.
We prefer the technique of combining an intercalary allograft with a vascularized fibular graft for arthrodesis after S234B or S2345B resections or for salvage of failed proximal humeral replacement prostheses (Table VI). In revisions, particular care must be taken to protect the neurovascular structures. Union of the vascularized fibular graft typically occurs within six months17. Clear radiographic evidence of allograft-host bone union can be delayedfor as long as a year at the distal junction. Rates of union appear higher after primary arthrodesis (four of five patients) compared with after secondary arthrodesis for failure of reconstruction with a proximal humeral replacement prosthesis (one of three patients). The rate of union after arthrodesis of the shoulder performed for non-tumor conditions in large series has been approximately 96 per cent (119 of 124)3,28.
Deep infection is a problem after arthrodesis with an intercalary allograft and a vascularized fibular graft, and one developed after one of five primary and two of three secondary procedures in our series. In two of the three patients who had an infection, another attempt at arthrodesis was successful. Fusion was achieved after the infected allograft was removed, the viable vascular fibular graft was retained, and a second vascularized fibular graft was subsequently placed. In reports of the early results of arthrodesis with an allograft after resection of a tumor, Gebhardt et al.15 and Peabody et al.26 noted no deep infection. Infection after a primary glenohumeral arthrodesis is uncommon3.
Fracture after an arthrodesis remains a risk. Of our ten patients in whom fusion was ultimately achieved after a primary or secondary osseous arthrodesis, four had a subsequent fracture. (Two had a stress fracture of the intercalary allograft; one, a complete fracture of dual vascularized fibular grafts; and one, a complete fracture of an intercalary allograft and a vascularized fibular graft.) Humeral fracture after glenohumeral arthrodesis was reported in eight (11 per cent) of seventy-one patients by Cofield and Briggs3 and in two (4 per cent) of fifty-three patients by Richards and Kostuik28. Mah and Hall21 reported no stress fractures in nine patients five to twenty-seven years after a primary arthrodesis that had been performed in childhood In an attempt to minimize the risk of fracture after arthrodesis, we refined our technique to include reinforcement of the medullary canal of the allograft with antibiotic-impregnated methylmethacrylate and overlap of the proximal and distal plates. More malleable pelvic reconstruction plates are also currently used29.
Discomfort after the arthrodesis was uncommon. Of the patients who had a successful fusion (after a primary or secondary procedure), seven reported no pain and three reported only mild or intermittent pain that was not disabling and that necessitated only intermittent use of anti-inflammatory or non-narcotic analgesics. Cofield and Briggs3 noted adequate relief of pain in forty-nine (74 per cent) of sixty-six adults after an arthrodesis, but Hawkins and Neer18 noted it in only eight of sixteen patients. Mah and Hall21 noted no pain in nine patients five to twenty-seven years after an arthrodesis.
Because of loosening, we no longer perform reconstruction with an implant to achieve prosthetic fusion in patients who have had an extra-articular resection. Saito et al.33 reported the use of a self-locking total shoulder prosthesis after extra-articular resection in two patients. However, because the patients died of disseminated disease after less than one year of follow-up, the conclusions that can be made about this type of implant are limited.
Options for reconstruction after S34 or S345 resections include an allograft-prosthetic composite, a proximal humeral replacement prosthesis, and an osteoarticular allograft. Advantages of reconstruction with a proximal humeral replacement prosthesis include immediate distal fixation, the ability to administer radiation therapy postoperatively, and a potentially lower risk of infection as compared with that associated with allografts. However, an unconstrained device can become unstable, leading to late failure of the implant1,32. Compared with a prosthesis, the principal advantage of an osteoarticular allograft is the ability to effectively reattach the tendons of the rotator cuff to corresponding tendon stumps on the allograft. Healing of these soft tissues restores active motion that typically is not achievable with prosthetic reconstruction. Potential complications with use of an allograft include delayed union or non-union at the host bone-allograft junction, fracture, and infection. The combined use of an allograft and a prosthesis (an allograft-prosthetic composite) offers the ability to reattach the functional soft tissues effectively while eliminating the potential for subchondral fracture or collapse.
In our series, the functional results were satisfactory for six patients who had had reconstruction with an osteoarticular allograft after an S34A resection but were more variable with proximal humeral replacement prostheses. In general, an osteoarticular allograft was selected for patients in whom the abductor mechanism was intact after resection and a proximal humeral replacement prosthesis was selected for those in whom it had been resected.
Reports in the literature have suggested that constrained proximal humeral replacement prostheses may yield better functional results than unconstrained prostheses after an S34 or S345 resection. Ross et al.32 reported less than 30 degrees of active flexion, extension, and abduction in twenty-four patients who had an unconstrained implant, with subluxation caudad to the coracoacromial arch in sixteen patients and dislocation cephalad to this level in three others. In a report on sixty patients who had a constrained implant, Capanna et al.2 reported an excellent over-all functional rating for 4 per cent, a good rating for 62 per cent, a fair rating for 30 per cent, and a poor rating for 4 per cent, according to the functional evaluation system of the Musculoskeletal Tumor Society. More than 60 per cent of the patients had a good rating with regard to motion and stability; however, only 6 per cent of these patients had good strength in abduction.
Gebhardt et al.16 reported on twenty patients who had had reconstruction with an osteoarticular allograft after an S34 or S345 resection. Twelve of eighteen patients who had been followed for a minimum of two years or until the graft failed had a good or excellent result on the basis of no evidence of disease, no pain, and function that was essentially normal or was limited only in terms of "recreational but not occupational activities." Two patients achieved active abduction to 90 degrees although most did not achieve more than 45 degrees. In our small series, two patients achieved more than 100 degrees of active abduction and four, between 60 and 75 degrees of abduction.
Subchondral fracture and collapse of an osteoarticular allograft is a serious complication, and it occurred in four of our eight patients by the most recent follow-up examination. Gebhardt et al.16 noted a subchondral fracture in four of twenty-one proximal humeral osteoarticular allografts after a minimum of two years. Volkov35 reported a 20 per cent rate of "collapse of the articular surface of the graft or of its deep part" in 105 patients one to nine years after insertion of a long-bone osteoarticular allograft.
Subchondral fracture of an osteoarticular allograft can be avoided with use of an allograft-prosthetic composite. Early reports on this method indicate that it has promise5,31; however, complications may become more evident with additional experience and longer durations of follow-up.
Loosening of the cemented intramedullary stem of a proximal humeral replacement prosthesis or a spacer has not been a problem in our experience. Stress at the bone-cement-stem interface may be minimized because of the limited function of the shoulder joint. Other authors also have reported no or low rates of failure of the stem2,4,23,32. Ross et al.32 noted some bone resorption at the prosthetic junction in six (30 per cent) of their twenty patients, a finding similar to our observation.
Continued effort must be made to develop new techniques and to refine existing methods for salvage of the limb in the treatment of malignant and destructive benign neoplasms of the shoulder girdle. It is hoped that the use of a uniform system of classification of resection and the functional results will be accepted and applied universally. Larger data pools can then be established to compare different methods of reconstruction for specific types of resection more effectively.
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Footnotes
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*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
Department of Orthopedic Surgery, Mayo Clinic Jacksonville, 4500 San Pablo Road, Jacksonville, Florida 32224. Please address requests for reprints to Dr. O'Connor.
Department of Orthopedics, Mayo Clinic and Mayo Foundation, Rochester, Minnesota 55905.
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N. Marina, M. Gebhardt, L. Teot, and R. Gorlick
Biology and Therapeutic Advances for Pediatric Osteosarcoma
Oncologist,
July 1, 2004;
9(4):
422 - 441.
[Abstract]
[Full Text]
[PDF]
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M. Manfrini, D. Vanel, M. De Paolis, C. Malaguti, M. Innocenti, M. Ceruso, R. Capanna, and M. Mercuri
Imaging of Vascularized Fibula Autograft Placed Inside a Massive Allograft in Reconstruction of Lower Limb Bone Tumors
Am. J. Roentgenol.,
April 1, 2004;
182(4):
963 - 970.
[Abstract]
[Full Text]
[PDF]
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M. R. DiCaprio and G. E. Friedlaender
Malignant Bone Tumors: Limb Sparing Versus Amputation
J. Am. Acad. Ortho. Surg.,
January 1, 2003;
11(1):
25 - 37.
[Abstract]
[Full Text]
[PDF]
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P. J. GETTY and T. D. PEABODY
Complications and Functional Outcomes of Reconstruction with an Osteoarticular Allograft After Intra-Articular Resection of the Proximal Aspect of the Humerus
J. Bone Joint Surg. Am.,
August 1, 1999;
81(8):
1138 - 46.
[Abstract]
[Full Text]
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