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Reverse shoulder arthroplasty for malignant tumors of proximal humerus
J Shoulder Elbow Surg (2015) 24, 36-44
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Reverse shoulder arthroplasty for malignant tumors of proximal humerus Nicolas Bonnevialle, MD, PhD*, Pierre Mansat, MD, PhD, Julie Lebon, MD, Jean-Michel Laffosse, MD, PhD, Paul Bonnevialle, MD Service d’Orthopedie–Traumatologie, Centre Hospitalier Universitaire de Toulouse-Purpan, Toulouse, France Background: Reverse shoulder arthroplasty (RSA) provides an alternative for shoulder girdle reconstruction after wide transarticular resection of the proximal humerus for malignant tumor. The aim of this study was to evaluate midterm outcomes of this therapeutic option. Methods: Ten patients with RSA were included and reviewed with 24 months of minimum follow-up. Proximal resection of malignant tumor included the ‘‘V’’ deltoid insertion in 4 patients. The humeral stem was coated (with an allograft in 2 patients and a cement mantel in 3) or left uncoated (5 patients). Results: At a mean follow-up of 42 months, among 8 prosthesis available for evaluation (2 patients died), the Constant and Murley score averaged 52 points, the 11-item version of the Disabilities of the Arm, Shoulder and Hand (QuickDASH) score averaged 29.5 points, the Subjective Shoulder Value averaged 58%, and the Musculoskeletal Tumor Society score averaged 20.25 points. Mean forward active elevation reached 122 , external rotation at side was 2 , and internal rotation was to L4. Three prostheses were unstable. The involvement of ‘‘V’’ deltoid insertion at surgery trended to worsen the clinical outcome. Atrophy of the anterior deltoid occurred in most of patients who had a previous transdeltoid biopsy. Radiographic evaluation found 1 stem loosening, 1 stem at risk, and 3 scapular notches without glenoid loosening. Conclusion: Use of RSA after resection of a malignant tumor of the proximal humerus seems to be an acceptable option to preserve function. However, radiographic evolution is worrisome, and long-term study remains necessary to validate this therapeutic option with follow-up. Level of evidence: Level IV, Case Series, Treatment Study. Ó 2015 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Tumor; allograft; reverse arthroplasty; shoulder
The proximal humerus is a common site of bone malignant tumor and secondary localizations.10 Even if the oncologic issue remains essential, preservation of shoulder
Ethical Committee Approval was not required for this study. Every patient agreed to the use of their clinical and radiographic data for scientific studies. *Reprint requests: Nicolas Bonnevialle, MD, PhD, Service d’Orthopedie–Traumatologie, Centre Hospitalier Universitaire de Toulouse–Purpan, Place du Dr Baylac, F-31059 Toulouse, France. E-mail address: [email protected] (N. Bonnevialle).
function is important for the patient after a wide resection of the proximal humerus and the rotator cuff tendons. Several techniques of shoulder reconstruction have been reported, including arthrodesis, allograft, and massive shoulder arthroplasties.2-4,11-13,15,17,19,22,23,28 The reverse shoulder arthroplasty (RSA) prosthesis offers an alternative therapeutic option when the rotator cuff tendons are included in the tumor resection. However, a prerequisite for this therapeutic option is the preservation of the axillary nerve and the deltoid muscle.5,12 Few studies in the literature have evaluated the results of RSA after tumor
1058-2746/$ - see front matter Ó 2015 Journal of Shoulder and Elbow Surgery Board of Trustees. http://dx.doi.org/10.1016/j.jse.2014.04.006
Reverse shoulder arthroplasty for tumors
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resection because the number of patients remains limited.31 We hypothesized that RSA is a reliable therapeutic option after resection of the proximal humerus and that an acceptable clinical outcome can be obtained. The aim of our study was to analyze the clinical and radiographic results after RSA for reconstruction of the proximal humerus in patients undergoing transarticular resection of a malignant tumor.
Material and methods Study characteristics A retrospective study was conducted in the University Hospital in our Orthopedic and Traumatology Department with a specialized Tumor Unit. Inclusion criteria were all patients treated for a malignant tumor of the proximal humerus with transarticular resection of the tumor and shoulder reconstruction with a RSA, who agreed to be part of the study, and who had a minimum of 2-year follow-up. Exclusion criteria were patients treated for a malignant tumor of the proximal humerus with transarticular resection of the tumor isolated or associated with shoulder reconstruction without a RSA, patients who would not agree to be part of the study, or those with a follow-up of less than 2 years.
Patient demographics From January 2006 to January 2010, 21 patients underwent operations for a malignant tumor of the proximal humerus in our specialized Tumor Unit. Eleven were excluded: 5 tumors (5 patients) were resected without reconstruction of the proximal humerus, and the reconstruction in 6 patients was performed with a hemiarthroplasty. The study included 10 patients (7 men and 3 women) who were an average age of 55 years (range, 28-82 years). The dominant shoulder was involved in 4 patients. Five patients were retired, 3 had a light-manual labor occupation, and 2 were heavy-manual workers. The malignant tumors were a chondrosarcoma in 4 patients, an intraosseous leiomyosarcoma in 1, a parosteal osteosarcoma in 1, and an isolated bone metastasis in 4 (3 from a kidney carcinoma and 1 from a breast cancer).
Therapeutic strategy and surgical procedure Diagnosis of the tumor was performed via a specimen obtained from a lateral transdeltoid surgical biopsy by our specialized tumor team. Treatment strategy was then decided by a multidisciplinary team, including orthopedic surgeons, radiologists, pathologists, and oncologists. Patients with osteosarcoma received neoadjuvant chemotherapy, 3 of 4 patients with metastasis received postoperative radiotherapy, and patients with chondrosarcoma or intraosseous leiomyosarcoma underwent surgical treatment alone. Two senior surgeons (P.B. and P.M.) performed the surgical procedure: one was specialized in oncology surgery and the other in shoulder replacement. All patients were placed in the beach chair position under general anesthesia and interscalene block. A deltopectoral approach was used. A separate excision of the biopsy scar and surrounding deltoid muscle was performed in
Figure 1 Classification of skeletal resection about the shoulder girdle according to the Musculoskeletal Tumor Society.16
continuity with the tumor. The cephalic vein was retracted laterally, and the pectoralis major tendon was released if necessary. The axillary nerve was systematically identified and respected during the procedure. The resection included the rotator cuff tendons and the proximal humerus, with a mean length of 10.5 cm (range, 7-13 cm). According to the Musculoskeletal Tumor Society (MSTS) classification system,16 resection was classified as S3 in 4 patients, S3S4 in 2, and S3S4S5 in 4 (Fig. 1). The distal humeral ‘‘V’’ deltoid insertion was preserved or slightly released from the humeral shaft in 6 patients (group 1) and was included in the resection for 4 patients (group 2). The shoulder was reconstructed with a RSA with a cemented stem in 10 patients: 7 Delta Xtend (DePuy Johnson & Johnson, Warsaw, IN, USA), one Delta 3 (DePuy Johnson & Johnson), and 2 Aequalis Reversed fracture system (Tornier, Montbonnot, France). The humerus was augmented with a nonirradiated bone allograft in 2 patients, and an allograft-prosthesis composite was performed. A plate was added between the allograft and the host bone to avoid any rotation. Gentamicin-impregnated cement mantel was preferred in 3 other patients to fill the gap secondary to bone resection. Finally, in the last 5 patients, no complementary system was needed, and a standard stem was used (4 stems were smooth and 1 stem had a hydroxyapatite layer coating). The glenoid baseplate was placed below the equator of the native glenoid and was fixed with 4 screws. An eccentric large glenosphere of 42 mm was used in all patients but 2, where a 38mm glenosphere was preferred. Specific attention was paid for humeral component positioning: retroversion was neutral in all patients, and the height of the stem reproduced the native humeral length. This was made by measuring precisely the resected part of the humerus (Fig. 2). If the ‘‘V’’ deltoid insertion or the latissimus dorsi, teres major, or pectoralis major tendons were involved, they were reattached onto the allograft or the cement mantel in an anatomic position with heavy nonabsorbable sutures. No muscle transfer was performed.
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Figure 2 (A) Tumor resection and allograft preparation. (B) Postoperative X-ray image shows the shoulder reconstruction with a reverse shoulder arthroplasty coated with an allograft (antirotational plate fixation).
Postoperative management The shoulder was immobilized postoperatively in a sling in internal rotation for 6 weeks. Most patients were allowed to immediately start the rehabilitation program of passive exercises under physiotherapist supervision. Active exercises were not introduced before 6 weeks. Patients were then encouraged to independently perform active exercises of the shoulder and arm and were allowed to perform light activities of daily living. A strengthening program was begun after 12 weeks.
Method of evaluation Patients were screened for postoperative recurrence of tumor or metastases at preset intervals in our Tumor Unit. Clinical and radiologic outcomes were assessed at 3 weeks, 6 weeks, 3 months, 6 months, and yearly thereafter. At the last follow-up, active and passive range of motion, including forward elevation, external rotation at the side, and internal rotation (defined as the spinous process reached by the thumb) were measured. A Hornblower’s sign and a lag sign in external rotation at the side were specifically looked for. Clinical results were evaluated with the Constant and Murley score,9 the 11-item version of the Disabilities of the Arm, Shoulder and Hand (QuickDASH) score,25 the Subjective Shoulder Value (SSV),20 and the MSTS score.16 Allograft integration, lucencies around the stem, and the existence of scapular notching, according to the Sirveaux classification29 were analyzed on plain radiographs (anteroposterior, scapular Y view, and axillary view).
Statistical analysis Even though the population studied was small, univariate descriptive statistics analysis was performed. Means were compared in the different patient groups; a t test was used for paired results, whereas unpaired results were compared with the
Mann-Whitney test. The significance level was set at .05. Statistical analysis was performed with SAS software (SAS Institute, Cary, NC, USA).
Results Mean follow-up was 42 months (range, 24-84 months).
Complications and additional procedures Complications and additional procedures are reported in Table I). Four complications occurred in 3 patients. An intraoperative brachial plexus injury was diagnosed postoperatively in patient 9, who had surgery for a chondrosarcoma. As a consequence, an anterior dislocation of the prosthesis occurred and led to surgical reduction without revision of the implant. No further dislocation occurred, and the neurologic deficit resolved spontaneously after 2 years (absolute Constant and Murley score: 59 points). Unfortunately, because of a combined local and systemic recurrence of the disease, the patient died 4 years after the index surgery. An anterior dislocation of the prosthesis occurred on day 3 in patient 10. In this patient, the tumor resection led to a 24-cm loss of bone diaphysis, and a massive allograft was used. A revision procedure was performed, adding a metallic tray (þ9 mm) and a thicker polyethylene liner (þ6 mm) to increase the length of the arm and the tension of the deltoid. The revision procedure failed, with recurrence of instability. Another revision was performed, and the RSA was converted to a hemiarthroplasty. At the 1-year follow-up, a disarticulation procedure was performed for
Reverse shoulder arthroplasty for tumors Table I
39
General data, technique of reconstruction used, and complications
Patient Age at Diagnosis surgery (y)
Resection Involvement Reconstruction Treatment technique complement (MSTS of ‘‘V’’ classification16) deltoid insertion
1
63
Kidney metastasis S3
2
47
3
82
Breast cancer S3S4 metastasis Kidney metastasis S3S4
4
78
Kidney metastasis S3
5
57
Chondrosarcoma
6
43
Intraosseous S3S4S5 leiomyosarcoma
7
36
Parosteal osteosarcoma
S3S4S5
8
45
Chondrosarcoma
S3S4S5
9)
75
Chondrosarcoma
S3
10)
28
Chondrosarcoma
S3 S4 S5
S3
No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem Yes-Group 2 RSA: long stem with allograft Yes-Group 2 RSA: long stem with cement mantel Yes-Group 2 RSA: long stem with cement mantel No-Group 1 RSA: standard stem
Radiotherapy
Yes-Group 2 RSA long stem with allograft
d
Postoperative Reoperation complication
d
d
Neoadjuvant d chemotherapy Radiotherapy d
d
Radiotherapy
d
d
d
d
d
d
d
d
Neoadjuvant d chemotherapy
d
d
d
Instability
d
Open reduction Brachial plexus palsy/ instability Instability 1st revision: RSA converted in hemiarthroplasty 2nd revision: disarticulation
d
MSTS, Musculoskeletal Tumor Society; RSA, reverse shoulder arthroplasty. ) Clinical results not available at follow-up because of death or removal of the RSA.
local tumor recurrence. The patient died 1 year later after systemic recurrence. A postoperative inferior dislocation was observed in patient 8. A simple brace was prescribed. Six months later, reduction was obtained with a stable prosthesis (Fig. 3). The Constant and Murley score reached 54 points.
Functional results At follow-up, 8 patients with the prosthesis still in place were available for examination by an independent observer. The mean absolute Constant and Murley score reached 52 points (range, 7-84 points), with an adjusted score of 61% (range, 10%-95%). The mean SSV was 58% (range, 10%95%), the QuickDASH score reached 29.5 points (range, 4.5-61.4 points), and the MSTS score reached 20.25 points (range, 7-29 points). The mean forward active elevation was 122 (range, 40 -170 ), external rotation at the side was 2 (range, 20 to 30 ), and internal rotation was to L4 (range, greater trochanter-T7). Functional results were
worse in the group 2 patients (with involvement of the distal deltoid insertion) than in group 1, without statistical significant difference (Table II). Clinically, all but 1 patient had a severe atrophy of the anterior part of the deltoid. All but 1 patient had a positive lag sign in lateral rotation at the side, and 2 patients in each group had a positive Hornblower’s sign. Among 3 patients who had a professional activity, 1 needed to change to a less demanding occupation.
Radiographic analysis Scapular notching was observed in 3 patients without glenoid loosening, and a glenoid spur was noted in 5 patients (Table III). Radiolucent lines around the stem were identified in 2 patients, and a humeral component was loose in another patient (Fig. 4). Resorption of the allograft was almost complete at follow-up (Fig. 5). Bone formation was observed around a proximal hydroxyapatite-coated implant (Fig. 6).
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Figure 3 Inferior instability (black arrows) is seen on immediate postoperative X-ray images (A and B). Relocation on X-ray images at 6-month follow-up (C and D).
Table II
Clinical results at last follow-up
Patient AAE ( ) group
Group 1 1 2 3 4 5 Mean Group 2 6 7 8 Mean P*
ER ( )
160 0 110 10 150 0 40 20 170 30 126 53 4 18
Constant and Murley score SSV (%) IR (vertebral Pain Activity Mobility Strength Absolute Adjusted level) total (%) (/15 pts) (/20 pts) (/40 pts) (/25 pts) total (/100 pts)
QuickDASH MSTS (/100 pts) (/30 pts)
T7 Sacrum GT GT T10 L3
80 20 T10 100 0 GT 170 20 GT 117 47 13 11 L4 .4 .1 .7
15 15 15 0 15 12 6.7
20 10 10 3 20 12.6 7
32 6 16 2 20 9 4 0 34 15 21 12 6.4 6
73 43 54 7 84 52 30
88 50 72 10 91 62 33.4
65 50 80 10 95 60 32.6
11.4 36.4 4.5 61.4 20.5 27 22.7
26 17 21 9 27 20 7.4
15 15 5 12 5.7 .47
10 16 17 14 3.8 .36
14 0 22 6 26 10 20.5 6 5.3 5 .47 .40
39 59 58 52 11.3 .49
53 64 64 60 6.3 .46
60 70 40 57 15 .44
38.64 29.5 34.1 34 4.7 .30
21 22 14 20.7 1.5 .88
AAE, active anterior elevation; ER, external rotation; group 1, without ‘‘V’’ deltoid involvement; group 2, with ‘‘V’’ deltoid involvement; GT, greater trochanter; IR, internal rotation; MSTS, the Musculoskeletal Tumor Society; pts, points; QuickDASH, 11-item version of the Disabilities of the Arm Shoulder and Hand; SSV, Simple Shoulder Value. NOTE. Mean data are presented as mean SD. ) Statistical analysis: group1 vs group 2 (P < .05 statistically significant).
Discussion RSA in case of wide transarticular proximal resection of the humerus for malignant tumor provides acceptable clinical outcomes and recovery of a functional shoulder. At followup, the mean objective adjusted Constant and Murley score and subjective SSV score were close to 60%. Worse results have been observed in patients in whom the resection
involved the distal humeral deltoid insertion. The complication rate was high, with instability of the prosthesis occurring in one-third of the patients. At only 42 months’ average follow-up, evolutive lucent lines were present on 2 of 8 humeral stems. RSA was initially indicated for cuff tear arthritis. Since then, indications have been expanded to primary arthritis associated with glenoid wear and nonfunctional rotator cuff
Reverse shoulder arthroplasty for tumors Table III
41
Radiographic analysis at last follow-up
Patient
Follow-up (mon)
Glenoid spur
Scapular notching (Sirveaux classification)29
Humeral stem coating
Humeral stem radiolucencies
1 2 3 4 5 6 7 8
36 24 24 43 84 32 42 52
No Yes Yes Yes Yes No No Yes
0 2 0 0 0 1 0 1
No coating No coating Hydroxyapatite No coating No coating Allograft Cement Cement
0 0 0 Yes 0 0 0 Loosening
Figure 4 (A) Immediate postoperative X-ray image shows a long cemented stem with cement mantel proximal coating. (B) X-ray image at 52 months of follow-up shows a stem loosening with radiolucent lines all around the stem and cortical bone erosion (black arrows).
muscles, fracture of the proximal humerus in elderly patients, and complex revision procedures for failed previous prostheses.5,21,26,30,31 The biomechanical principles of RSA are based on a stable fulcrum and an increasing deltoid lever arm.18,21 Results of RSA are not perfectly reproducible because they differ according to indications, the function of the remaining rotator cuff muscles, and the quality of the deltoid muscle.5,24,26,29-31 The largest series of RSA used after resection of the proximal humerus in the context of malignant tumor was reported by De Wilde et al.15 Reviewing 9 patients followed up an average of 7.7 years (range, 0.6-12 years), they concluded that this
procedure had a low morbidity and allowed recovery of adequate function for activities of daily living. Alternative therapeutic options after proximal humeral resection for tumor in adults were flail shoulder without any reconstruction, arthrodesis, massive allograft, or hemiarthroplasty. Recently, Bilgin3 described a technique of arthrodesis with a free vascularized fibula graft. Despite 2 major complications, bone fusion was achieved in 7 of 9 patients. However, the mean active flexion remained modest (80 ), and only 4 patients were able to reach their face and their hair. R€odl et al,28 in a comparative study of 45 patients with 2 years of follow-up, reported that
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Figure 5 X-ray images (A) postoperatively and (B) at 32 months of follow-up show a resorption of the allograft used to reconstruct the proximal bone resection.
Figure 6 Postoperative X-ray images show an atypical bone reconstitution (black arrows) around the proximal part of the stem at (A) 3 months and (B) at 1 year.
arthroplasty was the most reliable limb-salvage procedure. The same results were reported by Kassab et al,23 who recommended reverse composite arthroplasties in case of transarticular resection. Problems encountered after resection of the proximal humerus are represented by excision of the whole rotator cuff tendons that leads to an unbalance between the
external and internal rotator muscles. There are no more external rotators (infraspinatus and teres minor), whereas the pectoralis major, latissimus dorsi, and teres major are still functional to allow active internal rotation. Boileau et al6 have proposed to transfer the latissimus dorsi and teres major tendons onto the lateral side of the humeral implant to improve active external rotation (modified
Reverse shoulder arthroplasty for tumors L’Episcopo procedure). With this technique, results seem to show recovery of an active external rotation at the side and an improvement of the functional results.6,7,15,27 This procedure was not used in our series. Deltoid muscle involvement represents another problem to deal with after resection of the proximal humerus. It can be injured by the previous biopsy and also by the necessity to resect the biopsy track in continuity with the resected tumor. In some cases, for oncologic purposes, the distal insertion of the deltoid may be lifted off or included in the tumor resection. Even if postoperative range of motion tended to be worse in such a situation, deltoid impairment is not an absolute contraindication for RSA.24 Anterior deltoid atrophy was frequent in our series, probably because the biopsy track excision injured the anterior part of the axillary nerve. Using a more anterior approach for the biopsy, as close as possible to the deltopectoral approach, could be recommended to avoid deltoid impairment at the time of the resection. Humeral bone deficiency represents the third problem to deal with. Allograft-prosthesis composite has been proposed in case of revision surgery with a RSA to restore bone stock and maintain the height of the prosthesis and to improve primary stability.8,14 However, if this option seems valuable at short-term follow-up, the allograft will resorb unrelentingly with further follow-up, leaving the humeral stem suspended with cement alone at the proximal part.1,15,23 Instability of RSA has been shown to be the main complication of this procedure. Zumstein et al26 reported a rate of 4.7% of instability in a systematic review of RSA, whereas a 14% rate was reported by De Wilde et al15 after resection of the proximal humerus for tumor. In our series, 3 of 10 RSAs dislocated, probably because of involvement of the deltoid. No excessive shortening of the humerus was identified in these 3 patients. Humeral shortening has been reported to represent an usual problem after proximal humeral resection that could also lead to instability of the prosthesis.5,26 Measuring the resected proximal humerus and the opposite healthy humerus can prevent this complication. At the last follow-up, 8 of 10 patients in our study were considered as cured. One of these patients had radiologic signs of humeral loosening, radiolucencies around the stem were identified in another patient, and scapular notching was observed in 2 other patients. Loosening of humeral stem after primary replacement is rarely reported.31 However, at 85 months’ average follow-up, Kassab et al23 revised 2 among 7 RSAs for stem fracture or loosening after resection of the proximal humerus for tumor. The survival rate of RSA for tumors represents a limitation of this therapeutic option, especially in young patients, but these results must be compared with alternative therapeutic options. Weaknesses of this study are related to its retrospective characteristics and the low number of evaluated patients.
43 However, we have reported the results of a continuous single-center study in a specialized Tumor Unit with a standardized protocol. No patients were lost for follow-up.
Conclusion Use of RSA after resection of malignant tumor of the proximal humerus seems to be an acceptable option to restore a functional shoulder. Results depend on deltoid preservation as well as reconstruction of bone stock deficiency. However, the complication rate remains high, requiring revision surgery. An increased incidence of lucent lines around the humeral component, as well as scapular notching with follow-up, are of concern. However, RSA must be compared with alternative methods to restore a functional shoulder.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
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N. Bonnevialle et al. 21. Grammont P, Touilloud P, Laffay JP, Deries X. Etude et realisation d’une nouvelle prothese d’epaule. Rhumatologie 1987;30:407-18. 22. Hartigan DE, Veillette CJ, Sanchez-Sotelo J, Sperling JW, Shives TC, Cofield RH. Reconstruction of the proximal humerus for bone neoplasm using an anatomic prosthesis-bone graft composite. Acta Orthop Belg 2012;78:450-7. 23. Kassab M, Dumaine V, Babinet A, Ouaknine M, Tomeno B, Anract P. Twenty-nine shoulder reconstructions after resection of the proximal humerus for neoplasm with mean 7-year follow-up. Rev Chir Orthop Reparatrice Appar Mot 2005;91:15-23. 24. L€adermann A, Walch G, Denard PJ, Collin P, Sirveaux F, Favard L, et al. Reverse shoulder arthroplasty in patients with pre-operative impairment of the deltoid muscle. Bone Joint J 2013;95-B:1106-13. http://dx.doi.org/10.1302/0301620X.95B8.31173 25. Matheson LN, Melhorn JM, Mayer TG, Theodore BR, Gatchel RJ. Reliability of a visual analog version of the QuickDASH. J Bone Joint Surg Am 2006;88:1782-7. http://dx.doi.org/10.2106/JBJS.F.00406 26. Mizuno N, Denard PJ, Raiss P, Walch G. Reverse total shoulder arthroplasty for primary glenohumeral osteoarthritis in patients with a biconcave glenoid. J Bone Joint Surg Am 2013;95:1297-304. http://dx. doi.org/10.2106/JBJS.L.00820 27. Puskas GJ, Catanzaro S, Gerber C. Clinical outcome of reverse total shoulder arthroplasty combined with latissimus dorsi transfer for the treatment of chronic combined pseudoparesis of elevation and external rotation of the shoulder. J Shoulder Elbow Surg 2014;23:49-57. http:// dx.doi.org/10.1016/j.jse.2013.04.008 28. R€odl RW, Gosheger G, Gebert C, Lindner N, Ozaki T, Winkelmann W. Reconstruction of the proximal humerus after wide resection of tumours. J Bone Joint Surg Br 2002;84:1004-8. http://dx.doi.org/10. 1302/0301-620X.84B7.12989 29. Sirveaux F, Favard L, Oudet D, Huquet D, Walch G, Mole D. Grammont inverted total shoulder arthroplasty in the treatment of glenohumeral osteoarthritis with massive rupture of the cuff. Results of a multicentre study of 80 shoulders. J Bone Joint Surg Br 2004;86: 388-95. http://dx.doi.org/10.1302/0301-620X.86B3.14024 30. Young AA, Smith MM, Bacle G, Moraga C, Walch G. Early results of reverse shoulder arthroplasty in patients with rheumatoid arthritis. J Bone Joint Surg Am 2011;93:1915-23. http://dx.doi.org/10.2106/JBJS.J.00300 31. Zumstein MA, Pinedo M, Old J, Boileau P. Problems, complications, reoperations, and revisions in reverse total shoulder arthroplasty: a systematic review. J Shoulder Elbow Surg 2011;20:146-57. http://dx. doi.org/10.1016/j.jse.2010.08.001
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Reverse shoulder arthroplasty for malignant tumors of proximal humerus Nicolas Bonnevialle, MD, PhD*, Pierre Mansat, MD, PhD, Julie Lebon, MD, Jean-Michel Laffosse, MD, PhD, Paul Bonnevialle, MD Service d’Orthopedie–Traumatologie, Centre Hospitalier Universitaire de Toulouse-Purpan, Toulouse, France Background: Reverse shoulder arthroplasty (RSA) provides an alternative for shoulder girdle reconstruction after wide transarticular resection of the proximal humerus for malignant tumor. The aim of this study was to evaluate midterm outcomes of this therapeutic option. Methods: Ten patients with RSA were included and reviewed with 24 months of minimum follow-up. Proximal resection of malignant tumor included the ‘‘V’’ deltoid insertion in 4 patients. The humeral stem was coated (with an allograft in 2 patients and a cement mantel in 3) or left uncoated (5 patients). Results: At a mean follow-up of 42 months, among 8 prosthesis available for evaluation (2 patients died), the Constant and Murley score averaged 52 points, the 11-item version of the Disabilities of the Arm, Shoulder and Hand (QuickDASH) score averaged 29.5 points, the Subjective Shoulder Value averaged 58%, and the Musculoskeletal Tumor Society score averaged 20.25 points. Mean forward active elevation reached 122 , external rotation at side was 2 , and internal rotation was to L4. Three prostheses were unstable. The involvement of ‘‘V’’ deltoid insertion at surgery trended to worsen the clinical outcome. Atrophy of the anterior deltoid occurred in most of patients who had a previous transdeltoid biopsy. Radiographic evaluation found 1 stem loosening, 1 stem at risk, and 3 scapular notches without glenoid loosening. Conclusion: Use of RSA after resection of a malignant tumor of the proximal humerus seems to be an acceptable option to preserve function. However, radiographic evolution is worrisome, and long-term study remains necessary to validate this therapeutic option with follow-up. Level of evidence: Level IV, Case Series, Treatment Study. Ó 2015 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Tumor; allograft; reverse arthroplasty; shoulder
The proximal humerus is a common site of bone malignant tumor and secondary localizations.10 Even if the oncologic issue remains essential, preservation of shoulder
Ethical Committee Approval was not required for this study. Every patient agreed to the use of their clinical and radiographic data for scientific studies. *Reprint requests: Nicolas Bonnevialle, MD, PhD, Service d’Orthopedie–Traumatologie, Centre Hospitalier Universitaire de Toulouse–Purpan, Place du Dr Baylac, F-31059 Toulouse, France. E-mail address: [email protected] (N. Bonnevialle).
function is important for the patient after a wide resection of the proximal humerus and the rotator cuff tendons. Several techniques of shoulder reconstruction have been reported, including arthrodesis, allograft, and massive shoulder arthroplasties.2-4,11-13,15,17,19,22,23,28 The reverse shoulder arthroplasty (RSA) prosthesis offers an alternative therapeutic option when the rotator cuff tendons are included in the tumor resection. However, a prerequisite for this therapeutic option is the preservation of the axillary nerve and the deltoid muscle.5,12 Few studies in the literature have evaluated the results of RSA after tumor
1058-2746/$ - see front matter Ó 2015 Journal of Shoulder and Elbow Surgery Board of Trustees. http://dx.doi.org/10.1016/j.jse.2014.04.006
Reverse shoulder arthroplasty for tumors
37
resection because the number of patients remains limited.31 We hypothesized that RSA is a reliable therapeutic option after resection of the proximal humerus and that an acceptable clinical outcome can be obtained. The aim of our study was to analyze the clinical and radiographic results after RSA for reconstruction of the proximal humerus in patients undergoing transarticular resection of a malignant tumor.
Material and methods Study characteristics A retrospective study was conducted in the University Hospital in our Orthopedic and Traumatology Department with a specialized Tumor Unit. Inclusion criteria were all patients treated for a malignant tumor of the proximal humerus with transarticular resection of the tumor and shoulder reconstruction with a RSA, who agreed to be part of the study, and who had a minimum of 2-year follow-up. Exclusion criteria were patients treated for a malignant tumor of the proximal humerus with transarticular resection of the tumor isolated or associated with shoulder reconstruction without a RSA, patients who would not agree to be part of the study, or those with a follow-up of less than 2 years.
Patient demographics From January 2006 to January 2010, 21 patients underwent operations for a malignant tumor of the proximal humerus in our specialized Tumor Unit. Eleven were excluded: 5 tumors (5 patients) were resected without reconstruction of the proximal humerus, and the reconstruction in 6 patients was performed with a hemiarthroplasty. The study included 10 patients (7 men and 3 women) who were an average age of 55 years (range, 28-82 years). The dominant shoulder was involved in 4 patients. Five patients were retired, 3 had a light-manual labor occupation, and 2 were heavy-manual workers. The malignant tumors were a chondrosarcoma in 4 patients, an intraosseous leiomyosarcoma in 1, a parosteal osteosarcoma in 1, and an isolated bone metastasis in 4 (3 from a kidney carcinoma and 1 from a breast cancer).
Therapeutic strategy and surgical procedure Diagnosis of the tumor was performed via a specimen obtained from a lateral transdeltoid surgical biopsy by our specialized tumor team. Treatment strategy was then decided by a multidisciplinary team, including orthopedic surgeons, radiologists, pathologists, and oncologists. Patients with osteosarcoma received neoadjuvant chemotherapy, 3 of 4 patients with metastasis received postoperative radiotherapy, and patients with chondrosarcoma or intraosseous leiomyosarcoma underwent surgical treatment alone. Two senior surgeons (P.B. and P.M.) performed the surgical procedure: one was specialized in oncology surgery and the other in shoulder replacement. All patients were placed in the beach chair position under general anesthesia and interscalene block. A deltopectoral approach was used. A separate excision of the biopsy scar and surrounding deltoid muscle was performed in
Figure 1 Classification of skeletal resection about the shoulder girdle according to the Musculoskeletal Tumor Society.16
continuity with the tumor. The cephalic vein was retracted laterally, and the pectoralis major tendon was released if necessary. The axillary nerve was systematically identified and respected during the procedure. The resection included the rotator cuff tendons and the proximal humerus, with a mean length of 10.5 cm (range, 7-13 cm). According to the Musculoskeletal Tumor Society (MSTS) classification system,16 resection was classified as S3 in 4 patients, S3S4 in 2, and S3S4S5 in 4 (Fig. 1). The distal humeral ‘‘V’’ deltoid insertion was preserved or slightly released from the humeral shaft in 6 patients (group 1) and was included in the resection for 4 patients (group 2). The shoulder was reconstructed with a RSA with a cemented stem in 10 patients: 7 Delta Xtend (DePuy Johnson & Johnson, Warsaw, IN, USA), one Delta 3 (DePuy Johnson & Johnson), and 2 Aequalis Reversed fracture system (Tornier, Montbonnot, France). The humerus was augmented with a nonirradiated bone allograft in 2 patients, and an allograft-prosthesis composite was performed. A plate was added between the allograft and the host bone to avoid any rotation. Gentamicin-impregnated cement mantel was preferred in 3 other patients to fill the gap secondary to bone resection. Finally, in the last 5 patients, no complementary system was needed, and a standard stem was used (4 stems were smooth and 1 stem had a hydroxyapatite layer coating). The glenoid baseplate was placed below the equator of the native glenoid and was fixed with 4 screws. An eccentric large glenosphere of 42 mm was used in all patients but 2, where a 38mm glenosphere was preferred. Specific attention was paid for humeral component positioning: retroversion was neutral in all patients, and the height of the stem reproduced the native humeral length. This was made by measuring precisely the resected part of the humerus (Fig. 2). If the ‘‘V’’ deltoid insertion or the latissimus dorsi, teres major, or pectoralis major tendons were involved, they were reattached onto the allograft or the cement mantel in an anatomic position with heavy nonabsorbable sutures. No muscle transfer was performed.
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Figure 2 (A) Tumor resection and allograft preparation. (B) Postoperative X-ray image shows the shoulder reconstruction with a reverse shoulder arthroplasty coated with an allograft (antirotational plate fixation).
Postoperative management The shoulder was immobilized postoperatively in a sling in internal rotation for 6 weeks. Most patients were allowed to immediately start the rehabilitation program of passive exercises under physiotherapist supervision. Active exercises were not introduced before 6 weeks. Patients were then encouraged to independently perform active exercises of the shoulder and arm and were allowed to perform light activities of daily living. A strengthening program was begun after 12 weeks.
Method of evaluation Patients were screened for postoperative recurrence of tumor or metastases at preset intervals in our Tumor Unit. Clinical and radiologic outcomes were assessed at 3 weeks, 6 weeks, 3 months, 6 months, and yearly thereafter. At the last follow-up, active and passive range of motion, including forward elevation, external rotation at the side, and internal rotation (defined as the spinous process reached by the thumb) were measured. A Hornblower’s sign and a lag sign in external rotation at the side were specifically looked for. Clinical results were evaluated with the Constant and Murley score,9 the 11-item version of the Disabilities of the Arm, Shoulder and Hand (QuickDASH) score,25 the Subjective Shoulder Value (SSV),20 and the MSTS score.16 Allograft integration, lucencies around the stem, and the existence of scapular notching, according to the Sirveaux classification29 were analyzed on plain radiographs (anteroposterior, scapular Y view, and axillary view).
Statistical analysis Even though the population studied was small, univariate descriptive statistics analysis was performed. Means were compared in the different patient groups; a t test was used for paired results, whereas unpaired results were compared with the
Mann-Whitney test. The significance level was set at .05. Statistical analysis was performed with SAS software (SAS Institute, Cary, NC, USA).
Results Mean follow-up was 42 months (range, 24-84 months).
Complications and additional procedures Complications and additional procedures are reported in Table I). Four complications occurred in 3 patients. An intraoperative brachial plexus injury was diagnosed postoperatively in patient 9, who had surgery for a chondrosarcoma. As a consequence, an anterior dislocation of the prosthesis occurred and led to surgical reduction without revision of the implant. No further dislocation occurred, and the neurologic deficit resolved spontaneously after 2 years (absolute Constant and Murley score: 59 points). Unfortunately, because of a combined local and systemic recurrence of the disease, the patient died 4 years after the index surgery. An anterior dislocation of the prosthesis occurred on day 3 in patient 10. In this patient, the tumor resection led to a 24-cm loss of bone diaphysis, and a massive allograft was used. A revision procedure was performed, adding a metallic tray (þ9 mm) and a thicker polyethylene liner (þ6 mm) to increase the length of the arm and the tension of the deltoid. The revision procedure failed, with recurrence of instability. Another revision was performed, and the RSA was converted to a hemiarthroplasty. At the 1-year follow-up, a disarticulation procedure was performed for
Reverse shoulder arthroplasty for tumors Table I
39
General data, technique of reconstruction used, and complications
Patient Age at Diagnosis surgery (y)
Resection Involvement Reconstruction Treatment technique complement (MSTS of ‘‘V’’ classification16) deltoid insertion
1
63
Kidney metastasis S3
2
47
3
82
Breast cancer S3S4 metastasis Kidney metastasis S3S4
4
78
Kidney metastasis S3
5
57
Chondrosarcoma
6
43
Intraosseous S3S4S5 leiomyosarcoma
7
36
Parosteal osteosarcoma
S3S4S5
8
45
Chondrosarcoma
S3S4S5
9)
75
Chondrosarcoma
S3
10)
28
Chondrosarcoma
S3 S4 S5
S3
No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem No-Group 1 RSA: standard stem Yes-Group 2 RSA: long stem with allograft Yes-Group 2 RSA: long stem with cement mantel Yes-Group 2 RSA: long stem with cement mantel No-Group 1 RSA: standard stem
Radiotherapy
Yes-Group 2 RSA long stem with allograft
d
Postoperative Reoperation complication
d
d
Neoadjuvant d chemotherapy Radiotherapy d
d
Radiotherapy
d
d
d
d
d
d
d
d
Neoadjuvant d chemotherapy
d
d
d
Instability
d
Open reduction Brachial plexus palsy/ instability Instability 1st revision: RSA converted in hemiarthroplasty 2nd revision: disarticulation
d
MSTS, Musculoskeletal Tumor Society; RSA, reverse shoulder arthroplasty. ) Clinical results not available at follow-up because of death or removal of the RSA.
local tumor recurrence. The patient died 1 year later after systemic recurrence. A postoperative inferior dislocation was observed in patient 8. A simple brace was prescribed. Six months later, reduction was obtained with a stable prosthesis (Fig. 3). The Constant and Murley score reached 54 points.
Functional results At follow-up, 8 patients with the prosthesis still in place were available for examination by an independent observer. The mean absolute Constant and Murley score reached 52 points (range, 7-84 points), with an adjusted score of 61% (range, 10%-95%). The mean SSV was 58% (range, 10%95%), the QuickDASH score reached 29.5 points (range, 4.5-61.4 points), and the MSTS score reached 20.25 points (range, 7-29 points). The mean forward active elevation was 122 (range, 40 -170 ), external rotation at the side was 2 (range, 20 to 30 ), and internal rotation was to L4 (range, greater trochanter-T7). Functional results were
worse in the group 2 patients (with involvement of the distal deltoid insertion) than in group 1, without statistical significant difference (Table II). Clinically, all but 1 patient had a severe atrophy of the anterior part of the deltoid. All but 1 patient had a positive lag sign in lateral rotation at the side, and 2 patients in each group had a positive Hornblower’s sign. Among 3 patients who had a professional activity, 1 needed to change to a less demanding occupation.
Radiographic analysis Scapular notching was observed in 3 patients without glenoid loosening, and a glenoid spur was noted in 5 patients (Table III). Radiolucent lines around the stem were identified in 2 patients, and a humeral component was loose in another patient (Fig. 4). Resorption of the allograft was almost complete at follow-up (Fig. 5). Bone formation was observed around a proximal hydroxyapatite-coated implant (Fig. 6).
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Figure 3 Inferior instability (black arrows) is seen on immediate postoperative X-ray images (A and B). Relocation on X-ray images at 6-month follow-up (C and D).
Table II
Clinical results at last follow-up
Patient AAE ( ) group
Group 1 1 2 3 4 5 Mean Group 2 6 7 8 Mean P*
ER ( )
160 0 110 10 150 0 40 20 170 30 126 53 4 18
Constant and Murley score SSV (%) IR (vertebral Pain Activity Mobility Strength Absolute Adjusted level) total (%) (/15 pts) (/20 pts) (/40 pts) (/25 pts) total (/100 pts)
QuickDASH MSTS (/100 pts) (/30 pts)
T7 Sacrum GT GT T10 L3
80 20 T10 100 0 GT 170 20 GT 117 47 13 11 L4 .4 .1 .7
15 15 15 0 15 12 6.7
20 10 10 3 20 12.6 7
32 6 16 2 20 9 4 0 34 15 21 12 6.4 6
73 43 54 7 84 52 30
88 50 72 10 91 62 33.4
65 50 80 10 95 60 32.6
11.4 36.4 4.5 61.4 20.5 27 22.7
26 17 21 9 27 20 7.4
15 15 5 12 5.7 .47
10 16 17 14 3.8 .36
14 0 22 6 26 10 20.5 6 5.3 5 .47 .40
39 59 58 52 11.3 .49
53 64 64 60 6.3 .46
60 70 40 57 15 .44
38.64 29.5 34.1 34 4.7 .30
21 22 14 20.7 1.5 .88
AAE, active anterior elevation; ER, external rotation; group 1, without ‘‘V’’ deltoid involvement; group 2, with ‘‘V’’ deltoid involvement; GT, greater trochanter; IR, internal rotation; MSTS, the Musculoskeletal Tumor Society; pts, points; QuickDASH, 11-item version of the Disabilities of the Arm Shoulder and Hand; SSV, Simple Shoulder Value. NOTE. Mean data are presented as mean SD. ) Statistical analysis: group1 vs group 2 (P < .05 statistically significant).
Discussion RSA in case of wide transarticular proximal resection of the humerus for malignant tumor provides acceptable clinical outcomes and recovery of a functional shoulder. At followup, the mean objective adjusted Constant and Murley score and subjective SSV score were close to 60%. Worse results have been observed in patients in whom the resection
involved the distal humeral deltoid insertion. The complication rate was high, with instability of the prosthesis occurring in one-third of the patients. At only 42 months’ average follow-up, evolutive lucent lines were present on 2 of 8 humeral stems. RSA was initially indicated for cuff tear arthritis. Since then, indications have been expanded to primary arthritis associated with glenoid wear and nonfunctional rotator cuff
Reverse shoulder arthroplasty for tumors Table III
41
Radiographic analysis at last follow-up
Patient
Follow-up (mon)
Glenoid spur
Scapular notching (Sirveaux classification)29
Humeral stem coating
Humeral stem radiolucencies
1 2 3 4 5 6 7 8
36 24 24 43 84 32 42 52
No Yes Yes Yes Yes No No Yes
0 2 0 0 0 1 0 1
No coating No coating Hydroxyapatite No coating No coating Allograft Cement Cement
0 0 0 Yes 0 0 0 Loosening
Figure 4 (A) Immediate postoperative X-ray image shows a long cemented stem with cement mantel proximal coating. (B) X-ray image at 52 months of follow-up shows a stem loosening with radiolucent lines all around the stem and cortical bone erosion (black arrows).
muscles, fracture of the proximal humerus in elderly patients, and complex revision procedures for failed previous prostheses.5,21,26,30,31 The biomechanical principles of RSA are based on a stable fulcrum and an increasing deltoid lever arm.18,21 Results of RSA are not perfectly reproducible because they differ according to indications, the function of the remaining rotator cuff muscles, and the quality of the deltoid muscle.5,24,26,29-31 The largest series of RSA used after resection of the proximal humerus in the context of malignant tumor was reported by De Wilde et al.15 Reviewing 9 patients followed up an average of 7.7 years (range, 0.6-12 years), they concluded that this
procedure had a low morbidity and allowed recovery of adequate function for activities of daily living. Alternative therapeutic options after proximal humeral resection for tumor in adults were flail shoulder without any reconstruction, arthrodesis, massive allograft, or hemiarthroplasty. Recently, Bilgin3 described a technique of arthrodesis with a free vascularized fibula graft. Despite 2 major complications, bone fusion was achieved in 7 of 9 patients. However, the mean active flexion remained modest (80 ), and only 4 patients were able to reach their face and their hair. R€odl et al,28 in a comparative study of 45 patients with 2 years of follow-up, reported that
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N. Bonnevialle et al.
Figure 5 X-ray images (A) postoperatively and (B) at 32 months of follow-up show a resorption of the allograft used to reconstruct the proximal bone resection.
Figure 6 Postoperative X-ray images show an atypical bone reconstitution (black arrows) around the proximal part of the stem at (A) 3 months and (B) at 1 year.
arthroplasty was the most reliable limb-salvage procedure. The same results were reported by Kassab et al,23 who recommended reverse composite arthroplasties in case of transarticular resection. Problems encountered after resection of the proximal humerus are represented by excision of the whole rotator cuff tendons that leads to an unbalance between the
external and internal rotator muscles. There are no more external rotators (infraspinatus and teres minor), whereas the pectoralis major, latissimus dorsi, and teres major are still functional to allow active internal rotation. Boileau et al6 have proposed to transfer the latissimus dorsi and teres major tendons onto the lateral side of the humeral implant to improve active external rotation (modified
Reverse shoulder arthroplasty for tumors L’Episcopo procedure). With this technique, results seem to show recovery of an active external rotation at the side and an improvement of the functional results.6,7,15,27 This procedure was not used in our series. Deltoid muscle involvement represents another problem to deal with after resection of the proximal humerus. It can be injured by the previous biopsy and also by the necessity to resect the biopsy track in continuity with the resected tumor. In some cases, for oncologic purposes, the distal insertion of the deltoid may be lifted off or included in the tumor resection. Even if postoperative range of motion tended to be worse in such a situation, deltoid impairment is not an absolute contraindication for RSA.24 Anterior deltoid atrophy was frequent in our series, probably because the biopsy track excision injured the anterior part of the axillary nerve. Using a more anterior approach for the biopsy, as close as possible to the deltopectoral approach, could be recommended to avoid deltoid impairment at the time of the resection. Humeral bone deficiency represents the third problem to deal with. Allograft-prosthesis composite has been proposed in case of revision surgery with a RSA to restore bone stock and maintain the height of the prosthesis and to improve primary stability.8,14 However, if this option seems valuable at short-term follow-up, the allograft will resorb unrelentingly with further follow-up, leaving the humeral stem suspended with cement alone at the proximal part.1,15,23 Instability of RSA has been shown to be the main complication of this procedure. Zumstein et al26 reported a rate of 4.7% of instability in a systematic review of RSA, whereas a 14% rate was reported by De Wilde et al15 after resection of the proximal humerus for tumor. In our series, 3 of 10 RSAs dislocated, probably because of involvement of the deltoid. No excessive shortening of the humerus was identified in these 3 patients. Humeral shortening has been reported to represent an usual problem after proximal humeral resection that could also lead to instability of the prosthesis.5,26 Measuring the resected proximal humerus and the opposite healthy humerus can prevent this complication. At the last follow-up, 8 of 10 patients in our study were considered as cured. One of these patients had radiologic signs of humeral loosening, radiolucencies around the stem were identified in another patient, and scapular notching was observed in 2 other patients. Loosening of humeral stem after primary replacement is rarely reported.31 However, at 85 months’ average follow-up, Kassab et al23 revised 2 among 7 RSAs for stem fracture or loosening after resection of the proximal humerus for tumor. The survival rate of RSA for tumors represents a limitation of this therapeutic option, especially in young patients, but these results must be compared with alternative therapeutic options. Weaknesses of this study are related to its retrospective characteristics and the low number of evaluated patients.
43 However, we have reported the results of a continuous single-center study in a specialized Tumor Unit with a standardized protocol. No patients were lost for follow-up.
Conclusion Use of RSA after resection of malignant tumor of the proximal humerus seems to be an acceptable option to restore a functional shoulder. Results depend on deltoid preservation as well as reconstruction of bone stock deficiency. However, the complication rate remains high, requiring revision surgery. An increased incidence of lucent lines around the humeral component, as well as scapular notching with follow-up, are of concern. However, RSA must be compared with alternative methods to restore a functional shoulder.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
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