Treatment of Painful Pseudoparesis Due to Irreparable Rotator Cuff Dysfunction with the Delta III Reverse-Ball-and-Socket Total Shoulder Prosthesis

Werner, C.M.L. MD; Steinmann, P.A. MD; Gilbart, M. MD; Gerber, C. MD

Journal of Bone & Joint Surgery - American Volume: July 2005 - Volume 87 - Issue 7 - p 1476–1486
doi: 10.2106/JBJS.D.02342
Scientific Articles

Background: The Delta III reverse-ball-and-socket total shoulder implant is designed to restore overhead shoulder function in the presence of irreparable rotator cuff deficiency by using the intact deltoid muscle and the stability provided by the prosthetic design. Our purpose was to evaluate the clinical and radiographic results of this arthroplasty in a consecutive series of shoulders with painful pseudoparesis due to irreversible loss of rotator cuff function.

Methods: Fifty-eight consecutive patients with moderate-to-severe shoulder pain and active anterior elevation of <90° due to an irreparable rotator cuff tear were treated with a Delta III total shoulder replacement at an average age of sixty-eight years. Seventeen of the procedures were the primary treatment for the shoulder, and forty-one were revisions. The patients were examined clinically and radiographically after an average duration of follow-up of thirty-eight months.

Results: On the average, the subjective shoulder value increased from 18% preoperatively to 56% postoperatively (p < 0.0001); the relative Constant score, from 29% to 64% (p < 0.0001); the Constant score for pain, from 5.2 to 10.5 points (p < 0.0001); active anterior elevation, from 42° to 100° (p < 0.0001); and active abduction, from 43° to 90° (p < 0.0001). The patients for whom the implantation of the Delta III prosthesis was the primary procedure and those who had had previous surgery showed similar amounts of improvement. The total complication rate, including all minor complications, was 50%, and the reoperation rate was 33%. Of the seventeen primary operations, 47% (eight) were associated with a complication and 18% (three) were followed by a reoperation. Of the forty-one revisions, 51% (twenty-one) were associated with a complication and 39% (sixteen) were followed by a reoperation. Subjective results and satisfaction rates were not influenced by complications or reoperations when the prosthesis had been retained.

Conclusions: Total shoulder arthroplasty with the Delta III prosthesis is a salvage procedure for severe shoulder dysfunction caused by an irreparable rotator cuff tear associated with other glenohumeral lesions. Complications were frequent following both primary and revision procedures, but they rarely affected the final outcome. The procedure has a substantial potential to improve the condition of patients with severe shoulder dysfunction, at least in the short term.

Level of Evidence: Therapeutic Level IV. See Instructions to Authors for a complete description of levels of evidence.

1 Department of Orthopaedics, University of Zürich, Balgrist, Forchstrasse 340, 8008 Zürich, Switzerland. E-mail address for C. Gerber: christian.gerber@balgrist.ch

Article Outline

The treatment of irreparable rotator cuff tears associated with osteoarthritis of the glenohumeral joint is challenging1-3. Conservative treatment4, arthroscopic débridement5-7, replacement arthroplasty8-14, fusion, and resection arthroplasty15 have had variable results. Hemiarthroplasty provides partial pain relief3,10-12 but poor functional results16 and is therefore satisfactory only for elderly people with very low demands3,10-12. Total shoulder replacement has been shown to fail as a result of early glenoid loosening8-10. Fusion provides inconsistent pain relief and unsatisfactory function. Resection arthroplasty does not provide reliable pain relief and represents an ultimate salvage procedure of mainly historical interest15. The function of the Delta III inverted total shoulder prosthesis (Fig. 1), developed by Grammont17,18 in 1985, relies biomechanically almost entirely on the deltoid and thus does not depend on an intact rotator cuff. In contrast to other inverted total shoulder designs that have been proposed19-23, the Delta III prosthesis (DePuy France, Saint Priest CEDEX, France) not only medializes the center of rotation and lowers the deltoid muscle insertion, but also is of a semiconstrained design, all factors that might be responsible for the success of the implant. In the early experience with this device for the treatment of rotator cuff tear arthropathy, the functional results have appeared to be superior to those of hemiarthroplasty24.

The purpose of the current study was to evaluate the clinical and radiographic outcomes of arthroplasty with the Delta III prosthesis in a consecutive series of patients treated for painful pseudoparesis of the arm due to irreversible loss of rotator cuff function.

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Materials and Methods

Patients

Fifty-eight consecutive patients with painful pseudoparesis (defined as active shoulder elevation of <90° in the presence of free passive anterior elevation) caused by a massive irreparable rotator cuff tear were treated with the Delta III reverse-ball-and-socket total shoulder replacement. All patients gave their written consent prior to the procedure. Indications for surgery included severe pain, pseudoparesis, absence of overt septic arthritis, and an irreparable rupture of at least the supraspinatus tendon and either the subscapularis or the infraspinatus tendon. The rotator cuff was considered to be irreparable if the pseudoparesis was chronic, the acromiohumeral distance was <7 mm on a plain anteroposterior radiograph made with the shoulder in neutral rotation (Fig. 2-A), and fatty infiltration of the supraspinatus and infraspinatus muscles was greater than stage two according to the Goutallier classification25 (either on computed tomography scans or as adapted for magnetic resonance imaging by Fuchs et al.26).

There were fifteen men and forty-three women. Their mean age at the time of surgery was sixty-eight years (range, forty-four to eighty-four years). The dominant shoulder was involved in forty-four patients. Seventeen patients with cuff tear arthropathy had no previous operation (Group A), whereas, in forty-one patients, the implantation of the Delta III prosthesis was a revision procedure (Group B). Of the forty-one revisions, twenty-one were revisions of another prosthesis (Group B1): fifteen were revisions of a failed hemiprosthesis that had been used to treat a humeral head fracture; five, revisions of a failed total shoulder replacement that had been used to treat a humeral head fracture; and one, a revision of a failed hemiprosthesis that had been used to treat osteoarthritis. Twenty patients in the revision group had undergone a previous shoulder operation other than implantation of a prosthesis (Group B2): seventeen had had a previous reconstruction to treat a rotator cuff tear; two, arthroscopic débridement for a cuff tear; and one, open reduction and internal fixation as well as cuff reconstruction for a proximal humeral head fracture associated with a cuff tear.

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Surgical Technique and Postoperative Rehabilitation

All patients were operated on in a beach-chair position with use of general anesthesia, regional anesthesia, or a combination of both. A deltopectoral approach without detachment of the anterior aspect of the deltoid was used in all patients. In patients with a preserved subscapularis tendon, the superior part of the tendon was released from the lesser tuberosity. The axillary nerve was exposed and protected. The humeral resection guide was used to achieve <20° of humeral retroversion. After exposure of the glenoid, all soft tissues, including the long head of the biceps if it was present, and peripheral osteophytes were removed. The inferior aspect of the capsule and the long head of the triceps were released to provide space for the humeral component. The axis of the glenoid was determined, and the insertion point for the guide pin was chosen approximately 2 mm inferior to the middle of the glenoid and approximately centered anteroposteriorly18. Our ongoing clinical observations and a biomechanical investigation27 suggested that the optimal position for the convex glenoid component is more inferior than that suggested by the manufacturer and that this position can be obtained if the inferior border of the glenoid baseplate is flush with the inferior rim of the glenoid surface. The glenoid baseplate was therefore progressively shifted more distally, to this 2-mm inferior position, over the course of this study. Glenoid version was measured on preoperative computed tomography scans and corrected if necessary to 5° to 10° of retroversion with use of an adjustable guide pin. The humeral component was implanted with gentamicin-impregnated bone cement (Palacos; Essex Chemie, Lucerne, Switzerland) in forty-five patients and without cement in thirteen. The glenoid was replaced with a 36-mm glénosphère in fifty-six patients and with a 42-mm glénosphère in two. A standard lateralized humeral polyethylene cup was used in all patients. Suction drains were also used in all cases.

Physical therapy, consisting of passive and active-assisted exercises, was initiated immediately after the surgery. Passive and active mobilization in a pool was started immediately after removal of the suction drain, with the wound protected by an impermeable dressing. Between physical therapy sessions, the arm was kept in a sling. An abduction brace was never used. After two weeks, a free active range of motion was initiated as far as tolerated. Patients were encouraged to continue physical therapy sessions until six weeks after the index operation. This protocol is in contrast to the postoperative immobilization in an abduction splint for six weeks described by Grammont and Baulot18.

Clinical assessment was performed at a minimum of twenty-four months (average, thirty-eight months) postoperatively by two of us (C.M.L.W. and P.A.S.) who had not been involved in any of the surgical procedures. Like the prospectively performed preoperative examinations, the follow-up assessment consisted of a structured interview, clinical examination, photographic documentation, and radiographic evaluation. Also, the shoulders were assigned scores according to the system of Constant and Murley28, with use of the protocol previously described by one of us (C.G.)29, and the patients were asked to estimate the value of their shoulder as a percentage of an entirely normal shoulder (the subjective shoulder value30).

True anteroposterior, axillary lateral, and Neer scapular lateral radiographs were made under fluoroscopic control to assess component position, radiolucent lines, osteolysis, heterotopic ossification, and infrascapular notching. Inferior scapular notching was classified according to Nérot's system, as described by Valenti et al.31 and Sirveaux et al.32,33.

Statistical analysis of the results was performed with use of the Wilcoxon signed rank test (for comparison of specific preoperative and postoperative values), Spearman rank correlation (for correlation of outcome values with differences in the preoperative state of the shoulder and according to subgroups), and the Mann-Whitney U test (for analysis of differences between subgroups). As multiple comparisons between the groups were not performed, the Bonferroni-Dunn correction was not necessary to reduce the β error. The significance level was set at p ≤ 0.05.

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Results

Losses to Follow-up

At the time of follow-up, four patients had died from unrelated causes, three patients could not be reexamined because of their poor general health status, and one patient refused to be reexamined because of a poor clinical outcome (painful dysfunction with subluxation of the prosthesis). Thus, fifty patients were available for clinical follow-up.

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Complications and Failures (Table I)

The complication and failure rates were known for all fiftyeight patients, even though we were able to personally examine only fifty of them. Complications are therefore reported for the entire study group. A complication occurred in twentynine (50%) of the fifty-eight patients. The complication had an effect on the final outcome in six patients, as it led to removal of the prosthesis in two of them and to conversion to a hemiarthroplasty in four. The complication did not affect the final outcome in twenty-three patients. The majority of the complications occurred within a few weeks after the index operation. Nine complications occurred in eight of the seventeen patients who had undergone primary intervention (group A), thirteen complications occurred in twelve of the twenty-one patients who had had a revision of a prosthesis (group B1), and eleven complications occurred in nine of the twenty patients who had had a revision of a non-prosthetic procedure (group B2).

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Reoperations

Nineteen patients (33%) underwent a total of thirty-one (range, one to three) reoperations after implantation of the Delta III prosthesis. Eighteen percent (three) of the seventeen patients in group A, 38% (eight) of the twenty-one patients in group B1, and 40% (eight) of the twenty patients in group B2 had a reoperation.

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Failures

The six patients who had removal or conversion of the prosthesis were considered to have had a failure. Two of these patients were in group B1, and four were in group B2. No patient in group A had a complication necessitating removal or conversion of the prosthesis. Details of these six cases are summarized in Table I. Their functional results are not included with the reported results for the forty-four patients in whom the Delta III prosthesis was in situ at the time of the final follow-up.

In two patients, the prosthesis had to be removed because of an infection that had been unexpectedly identified by positive results of bacteriological cultures of intraoperative specimens. In one of these two patients, the prosthesis was replaced by a cement spacer one week after the index operation. Because of persistent fungal infection, however, the spacer was later removed and not replaced. In the other patient, the prosthesis was not reimplanted after removal of the prosthesis and implantation of a cement spacer because the patient had pain-free, subjectively satisfactory shoulder function. The patients both had a poor clinical outcome with relative Constant scores of 14% and 7% (10 and 5 points) at the time of follow-up; these scores corresponded to almost no shoulder function. However, the patients were pain-free and did not request additional surgical treatment.

In four patients, the prosthesis had to be converted to a hemiarthroplasty, as a result of loosening of the glenoid component in three and because of repeated anterosuperior dislocation of the prosthesis in one. The relative Constant scores for these patients were 23%, 57%, 75%, and 20% (17, 39, 48, and 14 points). Three of the patients had moderate pain, and one had severe persistent pain.

The most common complication, which did not affect the ultimate outcome, was postoperative hematoma, recorded for twelve patients. Aspiration of the hematoma alone was performed in five of these patients, and the other seven patients underwent open revision (partly because of concomitant complications requiring revision).

In addition to the patient who had the conversion to the hemiarthroplasty, as described above, four patients had anterosuperior dislocation of the prosthesis, which was attributed to insufficient soft-tissue tension and was recurrent in one of them. Closed reduction was the definitive treatment for one patient. The three remaining patients were treated successfully with surgical lengthening of the neck of the prosthesis by placement of a réhausseur, which is a 9-mm screw-in piece that can be added to the epiphysis of the prosthesis.

The polyethylene inlay dislocated and had to be revised in one patient. The polyethylene cup was replaced, following which a primary infection developed. It was necessary to temporarily remove the prosthesis and implant an antibiotic-impregnated cement spacer before the prosthesis was reimplanted. Three other patients (in addition to the two treated with prosthetic removal, as described above) had positive cultures and biopsies of specimens taken at the time of the index operation. The bacteriological examinations revealed coagulase-negative Staphylococcus in one case and Propionibacterium acnes in two. All three infections were successfully treated with intravenous antibiotics.

One axillary nerve lesion, which resolved completely, was recorded postoperatively. Another patient had a full loss of shoulder function due to persistent axillary nerve palsy following the resection of an intraspinal cervical ependymoma one year after the shoulder surgery. In another patient, progressive telescoping of an uncemented humeral component into the humeral shaft led to instability of the prosthesis. This patient underwent revision of the humeral component and implantation of a larger-diameter shaft with cement.

A fracture of the acromion or the scapular spine was recorded in four cases. These injuries were considered to be fatigue fractures of an eroded acromion or scapula and, in two patients, open reduction and internal fixation (tension band wiring) was necessary. The other two patients were successfully treated conservatively.

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Clinical Outcome (Table II)

Apart from the six patients who had a hemiarthroplasty or removal of the prosthesis, as reported above, and the one patient who refused to return for follow-up because of a poor clinical outcome, the patients had a high degree of satisfaction.

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Constant Score

The Constant score had at least doubled in all groups of patients in whom the prosthesis was still in place (forty-four patients), and was similar in the primary and revision groups. The mean relative Constant score increased from 29% preoperatively to 64% postoperatively (a gain of 35%, p < 0.0001) in the overall group, from 35% to 72% in group A, from 25% to 55% in group B1, and from 27% to 61% in group B2.

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Subjective Shoulder Value

The average subjective shoulder score approximately tripled in all three groups. It increased from 18% to 56% (a gain of 38%, p < 0.0001) in the overall group, from 19% to 59% (a gain of 40%) in group A, from 12% to 53% (a gain of 41%) in group B1, and from 23% to 52% (a gain of 29%) in group B2.

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Pain

The average Constant pain score (with 0 points indicating the most severe pain imaginable and 15 points indicating no pain) improved from 5.2 to 10.5 points (a gain of 5.3 points, p < 0.0001) overall. It improved from 6.2 to 12.3 points (a gain of 6.1 points) in group A, from 4.1 to 9.6 points (a gain of 5.5 points) in group B1, and from 5.6 to 8.9 points (a gain of 3.3 points) in group B2.

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Range of Active Motion

The average active anterior elevation increased from 42° to 100° (a gain of 58°, p < 0.0001) in the forty-four patients with the prosthesis in place. It increased from 43° to 103° in group A, from 39° to 96° in group B1, and from 44° to 97° in group B2. The average abduction increased from 43° to 90° (a gain of 47°, p < 0.0001) overall, from 39° to 84° in group A, from 43° to 95° in group B1, and from 47° to 91° in group B2. The average active external rotation with the arm at the side decreased from 17° to 12° (a loss of 5°, p = 0.04).

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Differences Between Subgroups

With the numbers available, no significant difference in the occurrence of complications, the subjective shoulder value, or patient satisfaction could be found between group A and group B or between group B1 and group B2. However, the rate of reoperations in group A (18%) was significantly higher than that in group B (39%) (p = 0.005). Also, there was a significant negative correlation between previous operations and the final Constant score, which averaged 72% in group A and 58% in group B (p = 0.03), and the postoperative pain score, which averaged 12.3 points in group A and 9.2 points in Group B (p = 0.01). The number of complications encountered did not appear to influence the overall satisfaction of the patients in whom the Delta III prosthesis had been preserved (p = 0.64).

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Radiographic Outcome

Radiolucencies were detected around parts of the humeral stem in eight patients (one in group A, three in group B1, and four in group B2). Seven of the stems were cemented, and one was uncemented. Only one stem (uncemented) was also clinically loose and had to be replaced. Radiolucent lines were found around the baseplate in five patients (Fig. 2-B); three baseplates were considered to be loose (with lucencies around the screws as well; Fig. 3). Notching of the inferior part of the scapular neck was found on 96% of the forty-eight follow-up radiographs that were available for interpretation (Figs. 2-B and 4). The notching did not extend to the inferior fixation screw of the implant (grades 1 and 2 according to the Nérot system reported by Sirveaux et al.32,33) in twenty-five cases (54%), and it reached or extended beyond the inferior screw (grades 3 and 4) in twenty-one cases (46%). The notching could not be correlated with any objective or subjective clinical result or complication. In thirty-eight (79%) of the forty-eight cases in which notching progression was analyzed on subsequent radiographs (Fig. 4), there was no enlargement of the osseous defect after one year. In half of those cases, the bone defect reached its final extent within a few months after implantation. In the ten patients with progression of the osseous defect, the notching had increased by a maximum of one grade according to the Nérot system32,33 at the time of the most recent follow-up.

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Discussion

The Delta III reverse-ball-and-socket shoulder prosthesis was developed by Grammont17,18 to restore shoulder function in the presence of an irreparable rotator cuff tear associated with glenohumeral osteoarthritis. As a result of the design of the implant, the center of rotation of the glenohumeral joint is medialized and the insertion of the deltoid muscle is moved distally. This increases the lever arm and the pretension of the deltoid muscle. The Delta III prosthesis can therefore address both the degenerative changes of the glenohumeral joint and the missing rotator cuff17,18,24,31-34.

All patients in our series had an irreparable rotator cuff tear and severe functional impairment, with active anterior elevation of the shoulder not exceeding 90° (so-called pseudoparesis). This functional impairment was associated with either degenerative changes of the glenohumeral joint (group A) or with previous shoulder surgery (group B), including total joint replacement. Both the subjective and the objective outcome values at a minimum of two years after the operation showed that the procedure had improved the patient's function substantially, with similar improvements in those treated with a primary arthroplasty and those treated with a revision. The operation resulted in a high degree of patient satisfaction when no complications requiring removal of the prosthesis had occurred. Whereas primary and revision arthroplasties resulted in similar improvements in the range of motion, the pain and relative Constant scores were significantly higher following the primary procedures. This finding is in contrast to that in the studies by Sirveaux et al.32,33, who reported that the Constant score was not influenced by previous surgery. The subjective shoulder value after implantation of the Delta III prosthesis was similar for all treatment groups in our study and was generally higher than the results reported following hemiarthroplasty12,14,35-40. However, patient satisfaction was low when the prosthesis had to be converted to a hemiarthroplasty or had to be removed.

Active external rotation was, as expected, not improved but actually decreased by a mean of 5° (p = 0.04). This finding reflects the inability of the deltoid to control external rotation, particularly in elevation and abduction41. The loss of active external rotation was also observed by Baulot et al.42, and patients should be informed about this outcome before the surgery. For patients with a severe external rotation lag and a torn teres minor, an additional tendon transfer29 might improve this function and is the subject of a current investigation.

The complication rate in our series is higher than previously reported rates18,24,31-34. One or more complications occurred in twenty-nine (50%) of the fifty-eight patients. In six patients, the complication required removal of the prosthesis or conversion to a hemiarthroplasty. The higher complication rate in our series might have been due to the fact that we considered hematoma formation, which occurred twelve times, to be a complication. This high rate of hematoma formation might be explained by the fact that (1) compared with conventional prosthetic designs, the reverse Delta-III design leaves a larger space free of soft-tissue after implantation, and (2) the initiation of postoperative physiotherapy before the wound has healed completely might favor hematoma formation. Another reason why the complication rate was high is that five infections that had not been apparent before the operation and were diagnosed with bacteriological examination of culture specimens obtained at the index operation were reported as complications. Finally, some complications were recorded separately even though they represented a single clinical event (e.g., loosening of the humeral component leading to dislocation of the prosthesis with a concomitant hematoma). Interestingly, in this series, in which the percentage of revisions was high (33%; nineteen patients), group-B patients did not have more complications than did group-A patients, but they did have a much higher rate of subsequent revisions, indicating that the complications were more serious in that group.

Subsidence of the humeral component was the reason for one revision. Because of this complication, we stopped implanting the humeral stem without cement. The manufacturer does not make any recommendations regarding the use of cement. Radiolucencies around the glenoid component were rare compared with the rates of glenoid radiolucency following conventional total shoulder arthroplasty8,43-47. This finding could be due to the fact that the glénosphère overlaps the baseplate32 by about 1 mm in situ and, therefore, small radiolucent lines could remain undetected even on perfectly oriented true anteroposterior radiographs. On the other hand, biomechanical analyses17 have suggested that shear forces at the interface between the baseplate and the scapula depend on the force developed by the deltoid in the absence of the rotator cuff. This force and the shear force on the implant both decrease as the lever arm of the deltoid increases. This is an advantage of the Delta III prosthesis and may explain the low rate of early glenoid failures compared with the rates associated with fixed-fulcrum designs.

Asymptomatic osteolysis at the distal part of the scapular neck, also referred to as notching, was observed in forty-six of the forty-eight patients with satisfactory follow-up radiographs (true anteroposterior views allowing correct grading with the Nérot system31). The lesion appeared rapidly after implantation and was stable after one year in thirty-eight (79%) of the patients. In contrast to the findings reported by Sirveaux et al.32, higher-grade (grade-3 or 4) notching did not correlate with lower Constant scores or any other clinical entity. Nérot31 proposed that grade-4 notching corresponds to glenoid loosening. In our patients, however, grade-4 notching was not associated with glenoid loosening. This finding might be due to the fact that the screws can still ensure stability even in the absence of contact between the baseplate and the glenoid bone (Fig. 4). We therefore think that additional radiolucencies around the screws are necessary to make a diagnosis of glenoid loosening with this prosthesis. Also, in contrast to the observation by Sirveaux et al.33, the radiographic presentation of grade-4 notching did not have the same congruent appearance as the lower-grade notching. Rather, it seemed to creep along the backside of the baseplate, as is seen in cases of osteolysis due to polyethylene wear. This finding was also reported by Nyffeler et al.48. Lateralization of the humeral component with use of a réhausseur (the additional epiphyseal part of the prosthesis) does not prevent the development of inferior scapular notching. It is, however, particularly useful when soft-tissue tension is lacking after implantation of the component. Also, the réhausseur can be used to lateralize the arm, allowing somewhat more adduction to occur, in shortbodied obese patients who have a very medialized scapula.

Although the etiology of inferior scapular notching remains unknown, the morphology of the lesion suggests a mechanical impingement between the polyethylene cup of the humeral component and the inferior bone of the scapular neck27,48.

Implantation of the glenoid component with an inferiorly tilted inclination might be considered in order to reduce impingement at the inferior aspect of the scapular neck. However, this would require reaming of the inferior aspect of the glenoid toward the lateral pillar of the scapular blade. The lateral border of the scapula would thereby be brought into direct contact with the adducted humeral component, and mechanical impingement would ensue. Furthermore, reaming in this fashion decreases the cortical substance left for implantation of the glenoid component and might be a factor predisposing to glenoid loosening27. The main factor associated with notching is positioning of the métaglène too superiorly on the glenoid, as was reported in detail by Nyffeler et al.27. It is important to recognize that the position recommended by the manufacturer (DePuy) does not correspond with the optimal position shown by testing and should not be used.

On the basis of the findings in this series, we concluded that the implantation of a Delta III prosthesis is a valuable procedure for the treatment of severe dysfunction of the shoulder due to an irreparable rotator cuff tear associated with glenohumeral pathology (degenerative osteoarthritis or prior surgery, including total shoulder replacement). However, because of the high complication rate and the fact that there may be long-term complications that are not yet known, arthroplasty with this implant should be reserved as a salvage procedure for situations in which an acceptable clinical outcome cannot be expected with another treatment modality.

Investigation performed at the Department of Orthopaedics, University of Zürich, Balgrist, Zürich, Switzerland

In support of their research or preparation of this manuscript, one or more of the authors received grants or outside funding from the ResOrtho Foundation, Zürich. None of the authors received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

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