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© 1999 The Journal of Bone and Joint Surgery, Inc. Complications and Functional Outcomes of Reconstruction with an Osteoarticular Allograft After Intra-Articular Resection of the Proximal Aspect of the Humerus* , CHICAGO, ILLINOISInvestigation performed at the Section of Orthopaedic Surgery and Rehabilitation Medicine, Department of Surgery, University of Chicago, Chicago
Background: The purpose of this study was to evaluate the functional outcome and the complications of reconstruction with an osteoarticular allograft in patients who had had intra-articular resection of the proximal aspect of the humerus. Methods: Sixteen patients who had had intra-articular resection and reconstruction of the proximal aspect of the humerus for the treatment of a tumor between 1986 and 1996 were evaluated. The length of the resected part of the humerus ranged from eight to 27.5 centimeters. The resections were classified as either S34A or S345A resections of the shoulder girdle on the basis of the Musculoskeletal Tumor Society classification system. Reconstruction was performed with use of a nonirradiated, frozen osteoarticular allograft with intact capsular and rotator cuff attachments. Dual orthogonal dynamic compression plates were used for internal fixation of the allograft to the host bone. The oncological parameters that were evaluated included survival of the patient, local recurrence, and metastasis. The radiographic parameters included time to union, stability of the joint, fracture of the allograft, and fragmentation of the epiphysis of the allograft (subchondral collapse). Survival of the graft was assessed with Kaplan-Meier survival analysis. The modified Musculoskeletal Tumor Society evaluation system was used to assess functional outcome. Results: At a median of forty-seven months (range, fourteen to 130 months) after the operation, fourteen of the patients in the study group were free of disease and two had died of disease. No patient had local recurrence or nonunion. Late complications included four fractures of the allograft and one infection of the graft. A Kaplan-Meier survival curve demonstrated a 68 percent rate of survival of the allograft at five years. Instability of the glenohumeral joint in the form of ptosis and anterior subluxation was noted in three patients, and dislocation of the glenohumeral joint was seen in eight patients. On the basis of the modified Musculoskeletal Tumor Society functional evaluation, the mean score at the most recent follow-up evaluation (at a mean of thirty-four months) was 70 percent. This score was lower than the mean score of 81 percent at a mean of fourteen months. All patients had normal manual dexterity and had mild or no pain at the most recent follow-up evaluation. However, all had restriction of recreational activities or partial disability in addition to limitations with regard to placement of the hand and the ability to lift. Conclusions: Reconstruction of the proximal aspect of the humerus with an osteoarticular allograft is an option that provides good relief of pain and preserves manual dexterity. However, in our study, function was limited by impairment of elevation of the shoulder and hand as well as by decreased strength of the shoulder. There was an extremely high rate of complications, including joint instability, fracture of the allograft, and infection of the allograft. We no longer routinely perform this reconstruction at our institution.
Limb-sparing resection is preferred to amputation in the operative treatment of primary malignant tumors or invasive benign tumors of the proximal aspect of the humerus9. Reconstructive procedures after such resections include the use of a prosthesis, a composite of an allograft and prosthesis, an osteoarticular allograft, or an arthrodesis with an allograft or an autogenous graft1,2,13,15. The type of reconstruction procedure that is used is often determined by the extent of the tumor13. Intra-articular tumors can be treated with an extra-articular resection in which the abductor mechanism, glenoid, and shoulder joint are resected en bloc with the tumor9. In contrast, tumors without extension into the joint can be treated with intra-articular resection, which allows partial or complete preservation of the deltoid muscle and rotator cuff tendons13. When the abductor mechanism has been preserved, reconstruction can be done with an osteoarticular allograft13. The benefit of this form of reconstruction compared with prosthetic reconstruction is that the attachment of the remaining deltoid muscle and rotator cuff tendons to the soft tissue of the allograft provides better potential for healing and function of the soft tissues. This form of reconstruction is thought to offer a patient the highest likelihood of active motion of the shoulder after resection of the proximal aspect of the humerus7. In this study, we analyzed the functional outcome and the complications of reconstruction with an osteoarticular allograft after intra-articular resection of the proximal aspect of the humerus.
We evaluated sixteen patients in whom a malignant tumor or an invasive benign tumor had been treated with intra-articular resection of the proximal aspect of the humerus and reconstruction with an osteoarticular allograft between September 1986 and June 1996. An incisional biopsy had been performed in ten patients and a needle biopsy, in four. The other two patients had been managed with primary resection on the basis of diagnostic radiographs. Five patients with osteosarcoma or Ewing sarcoma had received preoperative chemotherapy. No patient had received radiation therapy. In all patients, a wide intra-articular resection of the proximal aspect of the humerus was performed through a deltopectoral approach. In the patients who had had a previous biopsy, the site of the biopsy was excised along with a generous portion of the adjacent deltoid muscle, but in no patient was more than one-half of the deltoid muscle resected. The axillary nerve was preserved in three patients and was transected at the site of the anterior deltoid resection in thirteen. The length of the part of the humerus that was resected ranged from eight to 27.5 centimeters; the amount of the resection was chosen on the basis of preoperative axial computed tomography or magnetic resonance imaging. The resections were classified as either S34A or S345A resections of the shoulder girdle according to the Musculoskeletal Tumor Society classification system5. Specimens of bone marrow were obtained from the remaining portion of the humeral diaphysis for pathological evaluation and were found to be without tumor cells for all patients. Reconstruction was performed with a nonirradiated, frozen osteoarticular allograft consisting of the proximal aspect of the humerus with intact capsular and rotator cuff attachments. The allografts were obtained from regional bone banks. A particular allograft was chosen for each patient on the basis of estimates of bone size made from preoperative radiographs. A humeral head of equal or slightly smaller size than the host bone was selected. The allograft was secured to the host bone with use of two orthogonol dynamic compression plates and 4.5-millimeter cortical-bone and 6.5-millimeter cancellous-bone screws. Reconstruction of the soft tissues was performed by approximation of the host capsule and rotator cuff tendons to the allograft capsule and rotator cuff tendons with heavy nonabsorbable sutures. When possible, the deltoid-pectoralis major interval was repaired. Drains were placed. Postoperatively, the involved shoulder was kept in a flexed and abducted position in an abduction orthosis for six weeks, after which gentle active motion exercises were started. Care was taken to limit extension and external rotation of the shoulder. The database included demographic information, radiographs, operative reports, operative photographs, and pathology reports. Functional evaluations were based on the modified Musculosketetal Tumor Society functional evaluation system for the upper extremity6, which assesses pain, functional restrictions, emotional acceptance, positioning and dexterity of the hand, and lifting ability. Scores were determined by the attending physician or the clinical fellow at follow-up appointments throughout the postoperative course. The oncological parameters that were studied included survival of the patient, local recurrence, and metastasis. The radiographic parameters included time to union, stability of the joint, fracture of the allograft, and subchondral collapse. For the radiographic evaluation, fracture was defined as a discontinuity of the allograft bone in the metaphyseal-diaphyseal region; subchondral collapse, as fragmentation in the epiphyseal region; glenohumeral subluxation, as incongruent placement of the humeral head in the glenoid; and glenohumeral dislocation, as the complete lack of glenohumeral articulation. Radiographs from the most recent follow-up visit were reviewed, and early and late complications were described. Estimates of survival of the grafts were generated with Kaplan-Meier survival analysis (SAS Institute, Cary, North Carolina)8,14. Failure was defined as the removal of the allograft due to a complication such as fracture or infection.
The study group consisted of ten female and six male patients. The mean age was thirty-five years (range, ten to sixty-two years). Nine patients were diagnosed with chondrosarcoma (five stage-IA lesions, three stage-IB lesions, and one stage-IIB lesion3); four patients, with osteosarcoma (two stage-IIB and two stage-III lesions3); two patients, with giant-cell tumor of bone (both stage-3 lesions4); and one patient, with Ewing sarcoma (a stage-IIB lesion3). Of the sixteen patients in the study group, fourteen were free of disease at the time of oncological follow-up (mean, fifty-two months; range, fourteen to 130 months; median, forty-seven months). Two patients with stage-III osteosarcoma died of the disease fourteen months after the resection and reconstruction of the proximal aspect of the humerus. An additional patient was followed for only fourteen months because of failure of the allograft (Table I).
The only early complication was a deep venous thrombosis of the lower extremity with a nonfatal pulmonary embolus in one patient. Late complications included joint instability, fracture of the allograft, and infection of the allograft. Joint instability occurred in the form of early ptosis and inferior subluxation and later anterior dislocation (Figs. 1-A and 1-B). One allograft was revised because of infection, and four other allografts were revised because of metaphyseal fracture; no amputations were performed. All patients had prominent hardware related to resection or atrophy of the deltoid.
Results according to the modified Musculoskeletal Tumor Society functional evaluation6 were available for fourteen patients (Table II). One patient (Case 1) was not evaluated because he was followed at another institution, and another patient (Case 10) was not evaluated because the disease was progressing rapidly. When a patient had had a revision, we considered only the functional score that was assigned before failure of the graft and revision. The mean score for the fourteen patients who were evaluated was 70 percent at the time of the most recent follow-up (mean duration, thirty-four months; range, eleven to eighty-four months) (Table II). This score was lower than the mean score of 81 percent noted at a mean of fourteen months (range, two to thirty-five months) postoperatively. However, at the time of the most recent follow-up, all patients were satisfied (an emotional acceptance score of 3 of a possible 5 points), had normal manual dexterity, and had mild or no pain. However, all had limitation of recreational activities or partial disability. The major functional disabilities were limitations with regard to placement of the hand and lifting ability.
Of the nine patients who were alive and had the original osteoarticular allograft in place at the time of follow-up, three had anterior dislocation, three had anterior subluxation, and three had no instability, as demonstrated by physical examination. One of the patients who had a stable glenohumeral joint had had a resection of a benign giant-cell tumor with little soft-tissue resection. Another patient, who had an unstable joint, had had extensive resection of the rotator cuff and the deltoid, which left no meaningful muscle power acting across the glenohumeral joint. These cases highlight the concept that instability of the shoulder is not only a product of the reconstruction procedure; in most patients, it is related to the amount of soft tissue that was resected and the resultant alteration in the normal dynamics of the shoulder. The first patient had minimum alteration in the forces across the glenohumeral joint, whereas in the second patient nearly all muscular forces were eliminated. A review of the medical records of the nine surviving patients who did not have operative revision revealed severe limitations in the active range of motion of the glenohumeral joint. Often, the amount of active motion of the glenohumeral joint progressively decreased with time, especially in the patients who had subluxation or dislocation of the shoulder or fragmentation of the humeral head. The maximum active glenohumeral abduction in this group of patients was 40 degrees, and this was seen in the patient who had had resection of a benign neoplasm with preservation of most of the surrounding soft tissues. Four of the nine patients had no active glenohumeral abduction. Similar limitations in glenohumeral flexion and external rotation were noted. The five patients who had active glenohumeral abduction had sufficient strength to overcome gravity but not to overcome additional resistance. None of the nine patients were able to perform above-the-shoulder activities, and all had substantial difficulty with placement of the hand in an anterior and superior position because of limitations in strength and motion of the shoulder. Postoperative radiographs were reviewed for all sixteen patients in the study group at a mean of forty-eight months (range, four to 130 months) (Table III). Evidence of union was noted in all patients who were followed radiographically for at least six months. The mean time to union was sixteen months (range, six to thirty-eight months) (Table III). Metaphyseal fracture of the allograft occurred in four patients, at twelve, twenty, twenty-three, and seventy-two months. Two of these allografts had concurrent epiphyseal fragmentation (subchondral collapse). All fractures were proximal and occurred through a screw-hole in the allograft (Figs. 2-A and 2-B). Each fracture led to a revision with either a second osteoarticular allograft or a prosthetic reconstruction. A Kaplan-Meier survival curve8,14 demonstrated a 68 percent rate of survival of the allograft at five years (Fig. 3).
Thirteen of the sixteen patients were noted to have mild-to-severe resorption of the graft, typically in the region of the greater tuberosity beneath the lateral plate (Fig. 4). In twelve patients, the graft was less dense than the host bone. Four patients had severe resorption of the graft with epiphyseal fragmentation (subchondral collapse) (Fig. 5). Although revision was recommended to one patient who had epiphyseal fragmentation, no revisions were performed for this condition.
A review of the radiographs confirmed the clinical findings of glenohumeral instability in eleven patients; the radiographs demonstrated joint instability with anterior migration of the humeral head (Table III). Eight patients had anterior dislocation of the humeral head, whereas three had subluxation. Of the thirteen allografts followed for at least twenty months, only three remained stable. Changes consistent with arthritis of the glenohumeral joint or subchondral collapse of the humeral head were noted in seven of the sixteen patients. One of these seven patients had isolated glenoid arthritis, two had subchondral collapse of the humeral head, and four had both arthritis and subchondral collapse.
Limb-sparing resection is the preferred operative treatment of malignant primary tumors or invasive benign tumors of the proximal aspect of the humerus. In this study, we examined the functional outcome and the complications of one form of reconstruction after intra-articular resection of the proximal aspect of the humerus. The reconstruction procedure consisted of orthogonal plate fixation of an osteoarticular proximal humeral allograft to the host humerus with attachment of the capsular and rotator cuff soft tissues of the allograft to the host soft tissues. This reconstructive option was chosen for this group of patients because the intra-articular nature of the resection allowed preservation of the rotator cuff tendons. This form of reconstruction is thought to allow optimum function of the limb7. In a similar study published in 1990, Gebhardt et al.7 reported on a group of twenty patients in whom a primary malignant neoplasm or giant-cell tumor was treated with wide excision and reconstruction of the proximal aspect of the humerus with an osteoarticular allograft. The patients were followed for a mean of 5.3 years, and the allografts, for a mean of 4.5 years. Three of those patients had revision secondary to infection of the allograft, increasing the total number of reconstructions with an osteoarticular allograft to twenty-three. The complications associated with those twenty-three procedures included seven fractures, three infections, one nonunion, and one unstable shoulder. In addition, function was evaluated as described by Mankin et al.10. A rating of excellent was assigned if the patient was free of pain, had no evidence of recurrence, and had essentially normal function; good, if the patient was free of disease and pain and had no occupational limitations but did have limitation of recreational activities; and fair, if there was no evidence of recurrence but the patient used aids or supports because of pain or disability or was not capable of returning to the previous work status. The operation was considered to be a failure if the graft was removed or an amputation was performed because of a complication or recurrence or if the patient died secondary to disease. Gebhardt et al.7 used this system10 to evaluate function after eighteen initial reconstructions. At the time of follow-up, at a minimum of two years or until failure of the graft, they noted one excellent result, eleven good results, one fair result, and five failures (two were due to local recurrence and three, to infection of the allograft). However, of the eleven reconstructions with a good functional result, one had to be revised with an endoprosthesis because of fracture of the allograft. Three other patients who had a good functional result sustained a fracture; two of these fractures were treated with open reduction and internal fixation. Removal of a plate and open reduction and internal fixation secondary to nonunion was performed in another patient who had a good result. The patient who had a fair result sustained a fracture that was treated nonoperatively. Only seven of the eighteen patients had a good or excellent functional result with no complications related to the allograft, and only nine did not have a major second procedure. Still, the authors did not conclude that the complications precluded the use of this procedure. O'Connor et al.12 reviewed the results of treatment of a neoplasm of the shoulder in fifty-seven patients, with a median duration of follow-up of 4.6 years. Within that group, there were twelve resections that were comparable with those in the present study in that they involved only the proximal aspect of the humerus, with preservation of the abductor mechanism (S34A resections5). Of those twelve resections, seven were followed by reconstruction with an osteoarticular allograft; four, by insertion of an endoprosthesis; and one, by an arthrodesis. An additional reconstruction with an osteoarticular allograft was performed after a resection involving the axillary nerve, but the rotator cuff was preserved (an S34B resection). Of the eight patients who had reconstruction with an osteoarticular allograft, four sustained subchondral fracture or collapse; one of these fractures was treated with revision to an endoprosthesis. A fifth patient had a fracture at the metaphyseal-diaphyseal junction, which was revised with a second allograft. No instances of nonunion or instability were reported. The six patients (all managed with an S34A resection) who did not need revision were assessed with the modified Musculoskeletal Tumor Society functional evaluation6. The mean score was 71 percent, with the results reported to be satisfactory in all categories except function and positioning of the hand. The four patients who had reconstruction with a prosthesis had a mean score of 66 percent on the functional evaluation, and the one patient who was managed with arthrodesis had a score of 73 percent. O'Connor et al. concluded that the type of reconstruction should be chosen on the basis of the extent of the resection and the needs of the patient. They believed that reconstruction with an osteoarticular allograft is superior to prosthetic reconstruction after intra-articular resection with preservation of the abductor mechanism, but they noted subchondral collapse to be an associated problem. They suggested reconstruction with an allograft-prosthetic composite as a possible solution to subchondral collapse; however, no such procedures were included in their study. In the present study, fourteen patients were assessed with the modified Musculoskeletal Tumor Society functional evaluation6 at a mean of thirty-four months (median, thirty-one months). The mean score at that time was 70 percent, which is remarkably similar to the score noted by O'Connor et al.12. It is of interest that this score was lower than the maximum mean functional score, which was 81 percent at a mean of fourteen months postoperatively (Fig. 6). Most often, this decrease in the score was secondary to impairment of lifting ability or to increased functional restrictions and, to a lesser degree, to changes in pain or acceptance.
In addition to function decreasing over time, the prevalence of complications related to the graft increased. These complications included failure of the implant due to fracture or infection and epiphyseal fragmentation with subchondral collapse. Of the three patients who were followed for less than twenty months, one sustained a fracture. Of the thirteen patients who were followed for at least twenty months, three sustained a fracture and four had epiphyseal fragmentation (subchondral collapse). An additional patient in that group had revision because of infection. Only five of the thirteen patients who were followed for at least twenty months did not have a complication related to the allograft. Of the eight patients who were followed for more than forty months, only two had no complications related to the allograft. One of these two was the youngest patient in the group, and the other had a dislocated humeral head. These findings are in contrast with those of Mankin et al.10, who studied 106 patients managed with a wide resection of a malignant or an invasive benign tumor of an extremity followed by reconstruction with an osteoarticular or intercalary bone allograft. Sixty-one patients were followed for more than two years. Those authors found that if no complications occurred in the first two years, the grafts showed no evidence of progressive deterioration with time. Of the sixty-one reconstructions followed for more than two years, nine had been performed with an osteoarticular allograft of the proximal aspect of the humerus (one of which was a hemijoint graft). According to the authors' functional scale (described earlier), one result was scored as excellent; six, as good; and two, as failures (because of death). However, all nine of the functional evaluations were performed after the patient had had a reoperation, making it difficult to assess the result of the initial procedure. In a more recent publication, Mankin et al.11 reported on 818 allograft transplantation procedures (fifty-five of which involved an osteoarticular allograft of the proximal aspect of the humerus) and gave the results of 718 reconstructions (386 of which involved an osteoarticular allograft) that had been followed for more than two years. Of the 386 osteoarticular allografts, ninety-one (24 percent) were rated as excellent, 189 (49 percent) were rated as good, twenty-one (5 percent) were rated as fair, and eighty-five (22 percent) failed. Mankin et al. reported that few of the 718 reconstructions failed after the third year, with the exception of osteoarticular allografts of the lower extremities, which had failure of the articular surface approximately five years postoperatively. Allografts of the proximal aspect of the humerus were not discussed as a distinct group in that report. Instability was a problem in the current series, a finding that has not been commonly reported in previous studies7,10,12. In our group of sixteen patients, eight had a dislocated humeral head and three had a subluxation. Two of three reconstructions that were followed for twelve months or less remained stable, but only three of the thirteen reconstructions that were followed for longer than twelve months were stable. Again, an increased rate of complications was noted with longer follow-up. There was no clear relationship between instability and the level of axillary nerve transection. This joint instability, in the forms of anterior subluxation, anterior dislocation, and proximal migration, was progressive and debilitating. In the immediate postoperative period, the glenohumeral joint was noted to be reduced or slightly ptotic on radiographs and during physical examination. However, it appeared that, with time, attempted flexion of the shoulder recruited the long head of the triceps, the short head of the biceps, and the coracobrachialis. The contraction of these muscles, the progressive attenuation of the rotator cuff tendons, and the lack of an anterior aspect of the deltoid resulted in the humeral head being driven anteriorly and proximally. This dynamic deformity could have been corrected passively if treated early, but with time it became permanent. Once the humeral head was fixed in a position anterior and superior to the glenoid, the patients, although they had good motion at the elbow and manual dexterity, were unable to actively place the hand anteriorly to perform such functions as dressing, tending to personal hygiene, feeding themselves, using keys, opening doors, or shaking hands. Although this decrease in function was recorded with use of the functional rating system, the patients demonstrated a greater degree of disability than their scores reflected. High rates of patient satisfaction, excellent manual dexterity, and a painless extremity masked the patients' problems with activities of daily living. It is obvious that a more discerning and critical measure of function is necessary. In summary, our review of our experience with reconstruction of the proximal aspect of the humerus with an osteoarticular allograft after intra-articular resection with preservation of the abductor mechanism demonstrated a progressive decrease in function and an increased prevalence of complications related to the allograft with time. As reported in other studies7,12, fracture and epiphyseal fragmentation were noted to be common complications of this procedure. It may be that resorption and fracture are related to the mode of internal fixation and that use of alternative methods would decrease the prevalence of these complications. Unlike the findings in other studies, instability of the glenohumeral joint occurred in a high percentage of our patients. We believe that instability is due to resection of the anterior aspects of the deltoid, rotator cuff, and capsule with alterations in the dynamic forces on the shoulder. Also unique to the present study, to the best of our knowledge, was the demonstration that deterioration continued with time and that most of the failures of the allografts occurred more than one year postoperatively. The high rates of complications and reoperations reported in this and other studies, as well as the continued accrual of complications with time, have led us to abandon the routine use of this procedure and to consider other reconstructive procedures.
*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.
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