J Shoulder Elbow Surg (2015) -, 1-9

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Scapular allograft reconstruction after total scapulectomy: surgical technique and functional results Rodolfo Capanna, MDa, Francesca Totti, MDa, Ingrid C.M. Van der Geest, MD, PhDb, €ller, MDc,* Daniel A. Mu a

Department of Orthopedic Oncology, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy Department of Orthopedic Surgery, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands c Department of Orthopedic Surgery, University Hospital Balgrist, Zurich, Switzerland b

Hypothesis: Scapular allograft reconstruction after total scapulectomy preserving the rotator cuff muscles is an oncologically safe procedure and results in good functional outcome with a low complication rate. Methods: The data of 6 patients who underwent scapular allograft reconstruction after a total scapulectomy for tumor resection were retrospectively reviewed. At least 1 of the rotator cuff muscles was preserved and the size-matched scapular allograft fixed to the residual host acromion with a plate and screws. The periscapular muscles and the residual joint capsule were sutured to the corresponding insertions of the allograft. Results: The mean follow-up was 5.5 years (range, 24-175 months). In all patients, a wide surgical margin was achieved. The average functional scores were 20 points for the International Society of Limb Salvage score and 60 points for the American Shoulder and Elbow Surgeons score. Mean active shoulder flexion of 60 (range, 30 -90 ) and mean active abduction of 62 (range, 30 -90 ) were achieved. During the followup, 1 patient (16.6%) had a local recurrence and lung metastasis, whereas the remaining 5 patients (83.3%) were disease free. Two breakages of the osteosynthesis and 2 allograft fractures were observed, necessitating a revision surgery in 2 cases (33.3%). In this series, no infection, allograft resorption, or shoulder instability occurred. Conclusion: Allograft substitution of a completely removed scapula is an oncologically safe procedure, with good functional results, avoiding common complications in prosthetic replacements such as infection and dislocation of the shoulder joint. Level of evidence: Level IV, Case Series, Treatment Study. Ó 2015 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Scapula; scapulectomy; allograft; prosthesis; orthopedic oncology; limb salvage

This study was approved by our Institutional Review Board. *Reprint requests: Daniel A. M€uller, MD, Uniklinik Balgrist, Forchstrasse 340, CH-8008 Z€urich, Switzerland. E-mail address: [email protected] (D.A. M€uller).

Bone tumors in the scapula are a rare entity. Only 248 (3.2%) of all 7830 registered primary malignant bone tumors in the Rizzoli Institute database arise in the region of the scapula. The most common lesion is chondrosarcoma (52.4%), followed by Ewing sarcoma (27.4%) and osteosarcoma (12.9%).13

1058-2746/$ - see front matter Ó 2015 Journal of Shoulder and Elbow Surgery Board of Trustees. http://dx.doi.org/10.1016/j.jse.2015.02.006

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R. Capanna et al. Table I

Patient data

Patient

Sex

Age (years)

Diagnosis

Stage

Adjuvant therapy

Follow-up (months)

1 2 3 4 5 6

F F F M F M

43 36 38 46 47 41

CS SS CS LS CS CS

IA IIB IIB IIB IIB IIA

None CT and NRT None ACT and ART None None

175 82 59 31 27 24

CS, chondrosarcoma; SS, synovial sarcoma; LS, leiomyosarcoma; CT, neoadjuvant and adjuvant chemotherapy; ACT, adjuvant chemotherapy; NRT, neoadjuvant radiation therapy; ART, adjuvant radiation therapy.

The Enneking classification system for bone resections approved by the Musculoskeletal Tumor Society3 divides the scapula into 2 zones: segment 1 includes the scapular blade and spine; segment 2 contains the glenoid and acromion. Tumors affecting the whole scapula are demanding surgical situations not only to achieve an adequate margin but also to obtain a reconstruction with an acceptable upper limb performance. Scapulectomy and the Tikhoff-Linberg procedure7 have been used mainly to preserve the elbow and hand function. In both techniques, major impairments of the shoulder (restricted range of motion and instability) and a poor cosmetic outcome (flail arm) were reported.11,12 Most scapular tumors feature an extracompartmental extension requiring a complete resection of the periscapular muscles. In selected cases, however, the scapula may be removed, preserving some or even all of the muscles of the shoulder girdle. Therefore, several efforts have been made to improve the reconstruction by the use of prosthetic devices or massive allografts. Preliminary results of scapular prostheses showed an acceptable stability of the shoulder joint and a moderate active function.14,16-19 Long-term results have not been published yet. Osteoarticular acetabular allograft6 and scapular allograft reconstructions have been described and seemed to ensure moderate to good stability and function.2,9,10,20 After partial resection (segment 1 of the scapula, preserving the glenoid) and reconstruction of the scapular blade with an allograft, satisfactory results are usually obtained.20 However, the literature still remains sparse, especially concerning the use of a complete scapular allograft after a total scapulectomy. The purpose of this study was to present the current largest case series of 6 allograft reconstructions of the scapula after a total scapulectomy with preservation of the periscapular muscles and joint capsule. The patients were monitored during a mean follow-up of 66 months for complications as well as for oncologic and functional outcomes.

and 2012, 6 patients underwent a total scapulectomy with complete or partial preservation of periscapular muscles. An overall view of the patient data is given in Table I. The mean age at the time of surgery was 42 years (range, 36-47 years). In all cases, a preoperative biopsy and a complete histologic workup postoperatively were performed to classify the tumor type. In 4 patients (66.6%), the bone lesion was diagnosed as a chondrosarcoma, including 3 grade 2 lesions and 1 grade 1 lesion. In the remaining 2 patients, a soft tissue sarcoma was found: 1 (16.6%) synovial sarcoma and 1 (16.6%) leiomyosarcoma. The synovial sarcoma was treated by neoadjuvant chemotherapy and radiation therapy followed by surgical resection and adjuvant chemotherapy. The patient with leiomyosarcoma had previously had an intralesional resection in another hospital and was referred for further radicalization followed by adjuvant chemotherapy and radiation therapy. Plain radiographs, computed tomography scans, and magnetic resonance images of the shoulder girdle were used for local staging. Metastatic or skip lesions were excluded by the use of a technetium bone scan and total body computed tomography. All the patients had regular clinical follow-up visits including radiographic evaluation. Plain radiographs and computed tomography scans were used to detect nonunions or allograft fractures. As indicators of shoulder function, active flexion and abduction were measured. The International Society of Limb Salvage (ISOLS) score was calculated as well.4 This assessment consists of 6 different categories, for each of which a maximum of 5 points can be obtained (Table II). The total score is indicated either as points or percentage of the possible maximum score (30 points). The results were graded according to the following scale: excellent, 75% to 100%; good, 70% to 74%; moderate, 60% to 69%; fair, 50% to 59%; and poor, 5 cm or for those located in segment 2. Whenever the glenohumeral joint is preserved, good function of the arm can be expected.20 After a total scapulectomy, however, the future performance of the upper limb is poor.11,12 There are several reconstruction techniques to maintain some of the arm function after a total scapulectomy, including humeral suspension,1 scapular autograft2 or allograft,6 and prosthetic devices.18 An overview of the current literature concerning scapular allograft and scapular prosthesis is given in Tables VI and VII, respectively. After humeral suspension, in which the proximal humerus is simply stabilized with heavy nonabsorbable sutures or wires to the clavicle, the shoulder’s active range of motion and cosmetic results are always unsatisfactory.5 This technique was abandoned and remained a salvage procedure if no further reconstruction is possible. The prosthetic scapula devices show a better functional result than humeral suspension,14 but major issues in this

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R. Capanna et al. Table III

Resected muscles, oncologic outcome, and complications

Patient

Muscles resected

Surgical margins

Oncologic result

Complications

1 2 3 4 5 6

None Subscapularis None Infraspinatus, teres minor Supraspinatus, infraspinatus None

Wide Wide Wide Wide Wide Wide

CDF CDF CDF AWD CDF CDF

Failure of osteosynthesis Fracture of allograft None Fracture of allograft Failure of osteosynthesis None

CDF, currently disease free; AWD, alive with disease.

Table IV

ISOLS score and active range of motion

Patient

Pain

Function

Emotional acceptance

Hand positioning

Manual dexterity

Lifting ability

Total score

Flexion

Abduction

1 2 3 4 5 6 Mean

0 1 5 5 5 5 3.5

2 1 4 0 4 4 2.5

2 5 5 5 5 5 4.5

2 1 3 1 2 4 2.2

5 5 5 5 5 5 5

3 2 3 1 2 3 2.3

14 15 25 17 23 26 20

40 30 90 15 60 90 60

40 30 90 20 60 90 62

(47%) (50%) (83%) (56%) (76%) (87%) (66.7%)

The results for each patient as well as the mean value of the whole study group are indicated.

technique are shoulder joint instability and infections due to wound healing disturbances (Table VII). The use of an allograft reconstruction provides a better soft tissue reattachment and therefore lowers the risk for joint instability. However, the allograft can evoke structural problems, such as fractures or failures of the fixation to the host bone (Table VI). For alternative techniques, extracorporeally irradiated scapular autograft2 and acetabular allograft6 are described in the literature. No real advantage is found in use of an acetabular allograft. A size-matched scapular allograft allows complete restoration of the former anatomy, whereas an acetabular allograft creates a nonanatomic shoulder joint substitute. Reconstructions with autograft bone after tumor resections raise some doubts about the adequacy of achieved margins. In our experience, the adjuvant treatment applied to the bone, such as irradiation or cryotherapy, leads to structural weakness of the autograft with a higher fracture risk. This study focuses on the issues of allograft reconstruction after a total scapulectomy. Main limitations are the size of the study and the retrospective design. Although it is the largest series of its kind, it is difficult to draw conclusions based on a study with 6 patients. Our complication rate is comparable to that of other reports with allograft substitution of the scapula.2,9,10,20 There was no infection or shoulder instability, which is attributed to the fact that most of the periscapular muscles and the joint capsule were reconstructed in this series. Interestingly, common allograft failures, such as resorption

and joint degeneration, were not seen in this series, except a major osteoarthritis of the humeral head in 1 case after 10 years of follow-up without involvement of the glenoid. Scapular prostheses are linked to a higher rate of inadvertent events.14,16-19 Shoulder joint dislocations and infections, which seem especially to be a major problem with this kind of reconstruction, were completely avoided in our patients. The possibility of a solid reattachment of the muscle tendons is an important advantage of the allograft substitution. It is mandatory to keep the tendon insertions of the harvested scapula allograft to allow direct end-to-end sutures of the host and allograft tendons. Intraosseous sutures through drill holes should be avoided to reduce the risk of a subsequent allograft fracture. The use of frozen ( 80 C) allografts without any previous irradiation or autoclaving provides further stability. In our series, the only major revision surgery for a fracture was needed in the pretreated (liquid nitrogen) autograft. An internal fixation of the scapular allograft with a plate osteosynthesis between the posterior acromion and the spine of the scapula ensures a static stability of the allograft and therefore of the shoulder joint. In this series, breakage of the osteosynthesis happened 2 times (33.3%) shortly after the surgery. At the moment, no evident solutions are available to prevent this complication. Further studies should clarify whether restoration or reconstruction of the coronoid and trapezoid ligaments may reduce stress to the osteosynthesis and prevent failures. In 1 patient, the plate osteosynthesis was

Scapular allograft reconstruction after total scapulectomy Table V

7

ASES score consisting of the self-reported assessment of daily activities and evaluation of pain Patient 1

Activity Put on a coat Sleep on your affected side Wash back/do up bra in back Manage toileting Comb hair Reach a high shelf Lift 10 pounds above shoulder Throw a ball overhand Do usual work Do usual sport Total Pain Visual analog scale score (range, 0-10) Total score (maximum 100)

2

3

Mean 4

5

6

2 0 1 2 1 0 0 0 1 0 7

2 1 1 2 0 0 0 0 0 0 6

3 3 3 3 3 0 0 0 3 1 19

1 3 1 2 0 0 0 0 1 0 8

3 3 2 3 2 0 0 0 3 1 17

3 3 3 3 3 0 0 1 3 2 21

2.3 2.2 1.8 2.5 1.5 0 0 0.2 1.8 0.7 13

8 22

6 30

0 82

0 63

0 78

0 85

2.3 60

The results for each patient as well as the mean value of the whole study group are indicated.

Table VI Reported results in the literature for allograft reconstruction after total scapulectomy or resection of glenoid in comparison to the current study Author

Year

Patients

Reconstruction

Follow-up

Complications

ISOLS score

Range of motion

6

1998

2

2 Glenoid

33 months

None

90%

Mnaymneh10

2002

6

44 months

2009

3

26 months

1 Allograft fracture 1 Local recurrence 1 Chronic pain

82%

Zhang20

5 Total scapula 1 Glenoid 3 Glenoid

Abduction: 50 -75 Flexion: 40 -80 NA

79%

Chandrasekar2

2009

2

Merriman9

2010

Current study

2015

Lee

36 months

None

NA

1

2 Irradiated scapula autograft 1 Total scapula

61 months

None

NA

6

6 Total scapula

66 months

2 Osteosynthesis failures 1 Allograft fracture

66.7%

Abduction: 55 Flexion: 43 Abduction: 30 -60 Flexion: 30 -60 Abduction: 80 Flexion: 90 Abduction: 62 Flexion: 60

NA, not available.

changed immediately, and despite the minor revision surgery, good functional results were still reached. The other osteosynthesis failure without any revision developed 10 years later with osteoarthritis of the humeral head, whereas a possible relation remains dubious. Nevertheless, a prompt revision after osteosynthesis failure seems to work best. Regarding the soft tissue reconstruction, both the articular capsule and the deltoid muscle play the most important roles in shoulder stability and function. The articular capsule acts as a passive joint stabilizer and serves as a fulcrum for the shoulder abductor mechanism. The deltoid muscle is the predominant muscle in suspending the humerus, providing shoulder abduction and improving the

cosmetic contour of the shoulder.16 However, to restore shoulder function and to maintain shoulder stability, the rotator cuff, particularly the supraspinatus muscle, should also be preserved whenever possible. The careful preparation of supraspinatus and infraspinatus muscle flaps and conservation of the neurovascular bundle in the supraspinatus fossa are mandatory to maintain a satisfactory reconstruction result. In respect to the key features of the soft tissue reconstruction, the mean ISOLS score4 of the patients was 20 points (66.6%). The result seems to be lower than previously reported, but these studies included partial, subtotal, and total scapulectomy.2,9,10,20 Considering only the

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R. Capanna et al. Table VII

Reported results in the literature for scapular prostheses

Author

Year

Wittig19

2002

3

Schwab16

2006

19

Pritsch14

2007

15

Tang17

2011

10

Patients

Reconstruction

Follow-up

Complications

ISOLS score

Range of motion

Constrained prosthesis Constrained/ nonconstrained prosthesis Constrained/ nonconstrained prosthesis Constrained prosthesis

16 months

None

80%-90%

18 months

2 2 2 2 1

82%

Abduction: 25 -45 Flexion: 25 -45 NA

90 months

36 months

Infections Dislocations Wound necrosis Wound dehiscences Dislocation

1 Dislocation 1 Superficial infection

79%

76.6%

Abduction > 40 : 47% Flexion > 40 : 47% Abduction: 25 -45 Flexion: 25 -45

NA, not available.

patients with a resected glenoid, the functional score adjusts to our result (24 points). The active range of motion with flexion of 60 and abduction of 62 in this series is also close to the previous studies, even slightly better if only patients with a resected glenoid are considered. Also, in our experience, a preserved glenohumeral joint leads to much better active range of motion. A patient, who was not included in this study because of a subtotal scapulectomy and therefore intact glenohumeral joint, showed an excellent functional result after 137 months of follow-up. He achieved 30 points (100%) in the ISOLS score4 and full active flexion as well as abduction of 180 . In comparing the mean functional results to the published values of prosthetic replacements, no evident differences were found.14,16-19 However, with use of a prosthetic device, the active flexion and abduction almost never were above 60 , whereas with the presented allograft technique, all 3 patients (50%) surpassed the limit of 60 both in flexion and in abduction. In respect to only the first 10 years of follow-up, even 4 patients (66.6%) in our series achieved a flexion and abduction above 60 , so the upper limit of the possible functional performance of the allograft reconstruction is higher. In our experience, a partial scapulectomy involving only segment 1 is best reconstructed by an allograft substitute, simplifying the reattachment of the muscles. If segment 2 or the total scapula has to be removed, a prosthetic or allograft replacement is possible. With use of a scapular prosthesis, the reinsertion of the muscles is difficult to maintain, and only a Trevira tube can restore the absent joint capsule. All these factors lead to a lower function and a higher instability rate. The allograft reconstruction can avoid the instability problem by suturing the remaining host capsule to the graft capsule and by careful positioning of the scapula on the chest wall, respecting the physiologic angles. The functional results depend highly on rotator cuff preservation. If the supraspinatus muscle and, further, the infraspinatus or the subscapularis muscle are spared, good to excellent shoulder function can be expected. The entire

resection of the rotator cuff is not a contraindication to a scapular allograft but may require other significant variations in technique to be successful.

Conclusion Substitution of the scapula with a massive allograft in case of a total scapulectomy is an oncologically safe procedure with an acceptable complication rate. Preservation of flexion and abduction of the rotator cuff muscles up to 90 is feasible in optimal cases, avoiding common problems of a scapular prosthesis, such as infection and shoulder dislocations.

Disclaimer The authors, their immediate families, and any research foundation 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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