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DOI:10.2214/AJR.07.3286
AJR 2008; 191:482-489
© American Roentgen Ray Society


Pictorial Essay

En Bloc Shoulder Resection with Total Shoulder Prosthetic Replacement: Indications and Imaging Findings

Rinat Masamed1, Thomas J. Learch2 and Lawrence R. Menendez3

1 Department of Radiological Sciences, David Geffen School of Medicine at UCLA, University of California, Los Angeles, Center for the Health Sciences, 10833 Le Conte Ave., Los Angeles, CA 90095.
2 Department of Radiology, Cedars-Sinai Medical Center, Los Angeles, CA 90048.
3 Department of Orthopaedics, Keck School of Medicine of the University of Southern California, Los Angeles, CA 90033.

Received October 13, 2007; accepted after revision February 7, 2008.

 
All prostheses manufactured by Stryker Orthopaedics (formerly Howmedica Osteonics).

Address correspondence to R. Masamed.


Abstract
Top
Abstract
Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 
OBJECTIVE. Our purpose was to highlight the importance of radiologic studies in assessing the appropriateness of total scapular resection and total shoulder prosthetic reconstruction and to examine the role of imaging in evaluating for postoperative complications.

CONCLUSION. Evolving surgical and reconstructive techniques for treatment of shoulder girdle tumors require radiologists to familiarize themselves with novel imaging findings associated with these procedures. Readers will better understand the indications for limbsparing surgery with total shoulder prosthetic reconstruction, normal postoperative radiologic findings, and common complications.

Keywords: en bloc shoulder resection • prosthesis • scapula • shoulder girdle • Tikhoff-Linberg resection


Introduction
Top
Abstract
Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 
Sarcomas compose less than 1% of all adult and 15% of pediatric malignancies [1], the shoulder girdle being a relatively common site for these malignant tumors. Chondrosarcomas are the most common primary malignancy of the scapula, although 12% occur in the proximal humerus, which is also the third most common site for osteosarcomas. Ewing sarcomas occur in the proximal humerus 7% of the time, and in the scapula 4–5% of the time [2]. Thirteen percent of soft-tissue sarcomas occur in the upper extremities [1]. The shoulder girdle is also a common area for metastases.

Dramatic change has occurred in the treatment of shoulder girdle neoplasia. Forequarter amputation (removal of the upper extremity including the scapula and clavicle) was once the treatment of choice. Today, most shoulder girdle tumors are treated with limbsparing procedures such as the Tikhoff-Linberg procedure. The operation consists of removal of the scapula, humeral head, outer third of the clavicle, and surrounding soft tissue. Modern techniques involve total shoulder prosthetic reconstruction to achieve maximal function of the salvaged upper extremity. Depending on the extent of involvement of the osseous and soft-tissue structures surrounding the shoulder, other surgical options may include intraarticular proximal humeral resection, partial scapulectomy, intraarticular total scapulectomy, or extraarticular humeral and glenoid resection [1]. The focus of this pictorial essay is the Tikhoff-Linberg procedure (extraarticular proximal humeral, distal clavicular, and total scapular resection) with total shoulder prosthetic reconstruction. Published reports documenting imaging findings both pre- and postoperatively are limited. In this pictorial essay, we give an overview of these important radiologic findings.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 
A retrospective chart and film review was performed of 13 patients who underwent the Tikhoff-Linberg procedure with total shoulder prosthetic reconstruction at the authors' institution over a 6-year period from 1999 to 2005. The types of tumors treated included five chondrosarcomas (four scapular and one proximal humeral), two Ewing sarcomas, one pleomorphic leiomyosarcoma, three metastatic renal cell carcinomas, one metastatic uterine leiomyosarcoma, and one metastatic melanoma. All patients underwent preoperative anteroposterior scapula, transscapular oblique, and humeral anteroposterior internal–external rotation conventional radiography. CT or MRI or both of the affected shoulder were performed in addition to any staging imaging performed to assess the extent of disease. Postoperative conventional radiography with similar technique was performed within 1 week after surgery, as well as at 1- to 6-month intervals depending on the patient's particular situation. Dedicated advanced imaging of the postsurgical site was ordered a few weeks postoperatively to serve as a baseline study. In addition, CT, MRI, and nuclear medicine studies were performed on an as-needed basis for detailed evaluation of complications and disease recurrence.


Protocols
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Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 
The most frequently requested advanced postoperative imaging techniques include CT and MRI. CT of the chest is obtained to evaluate for metastatic disease. Routine chest protocols are used. The prosthesis is imaged on these examinations. The affected arm is usually at the side because of difficulty in positioning it overhead.

Dedicated advanced imaging of the postsurgical site is ordered a few weeks postoperatively to serve as a baseline study for comparison for all future studies. Both MRI and CT examinations have inherent limitations because of metallic artifact. Both studies may be ordered and can be additive and complementary. CT is particularly valuable at assessing alignment of the scapular–humeral component articulation and periprosthetic fractures of the humeral stem. MRI excels at assessment of surrounding soft-tissue abnormalities such as tumor recurrence, lymphadenopathy, and postoperative fluid collections. These problems may also be identified on CT.

For CT, the opposite arm is positioned above the head. The affected arm is placed at the side with the palm next to the thigh in a comfortable position. The patient is placed in the gantry so that the area of interest is as close to the center of the gantry as possible. The field of view is chosen to cover the lateral chest, axilla, shoulder, and proximal humerus; 1-mm-thick transverse slices with 50% overlap are obtained; mA is increased to 400; and kV is increased to 140.

MRI protocols are designed to reduce and minimize metal artifact. This includes T1 and inversion sequences using fast spin-echo, high echo-train lengths (9–19), and the highest bandwidth possible (300 kHz and above). Phase and frequency encoding are planned to deflect artifact away from area of interest. If IV gadolinium is used, T1-weighted sequences are used. Fat saturation is not attempted because of the large amount of metal.

Review of these imaging studies helped identify important preoperative imaging techniques and findings that would assess the appropriateness of this procedure for a particular patient. In addition, common complications were recognized based on postoperative image review.


Results and Discussion
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Abstract
Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 
The following is a pictorial representation of the information gleaned from the chart and film review of this group of patients as well as a review of the literature regarding this limb-salvage procedure.

Indications, Contraindications, and Preoperative Imaging Studies
Imaging plays an important role in deciding whether the Tikhoff-Linberg procedure is appropriate for a given patient. In his 1928 paper, Boris Edmunovich Linberg [3], a Russian surgeon, proposed three uses for this limb-sparing operation. The first was for the treatment of malignant tumors of the proximal humerus, scapula, or clavicle that have likely invaded all parts of the shoulder and its joints (Figs. 1A, 1B, and 2). The second was removal of tumors that do not involve the axillary neurovascular bundle (Figs. 2 and 3). And the third was operations that had potential results equivalent to or better than amputation, with preservation of good elbow and hand function [3]. As previously shown, preoperative imaging including conventional radiographs, and particularly CT or MRI, is needed to assess the extent of tumor involvement because the Tikhoff-Linberg procedure is absolutely contraindicated when the tumor involves the axillary neurovascular bundle due to a high risk of recurrence. Relative contraindications include tissue contamination at biopsy, pathologic fracture, and chest wall invasion, although a patient in our series with chest wall involvement underwent a successful operation without recurrence at 12-month follow-up [1] (Figs. 4A and 4B). In addition, preoperative CT or MRI can help estimate whether there will be enough soft tissue remaining for the reconstruction.


Figure 1
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Fig. 1A 44-year-old woman with chondrosarcoma of right proximal humerus. Anteroposterior radiograph shows destructive lesion of right proximal humerus with wide zone of transition containing chondroid matrix.

 

Figure 2
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Fig. 1B 44-year-old woman with chondrosarcoma of right proximal humerus. Axial inversion recovery MR image shows lobular extension of mass into surrounding soft tissues and glenohumeral joint. Note encasement of long head of biceps tendon (arrow) and articular extension, indicating extraarticular resection by means of Tikhoff-Linberg procedure.

 

Figure 3
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Fig. 2 29-year-old man with chondrosarcoma of right scapula. Axial IV contrast-enhanced CT scan reveals that scapular tumor (black arrow) does not involve axillary neurovascular bundle (white arrow), making Tikhoff-Linberg procedure a safe limb-sparing option.

 

Figure 4
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Fig. 3 33-year-old man with right scapular chondrosarcoma. Axial T1-weighted MR image shows scapular chondrosarcoma with central necrosis (arrow) that has not invaded axillary neurovascular bundle.

 

Figure 5
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Fig. 4A 33-year-old man with right scapular chondrosarcoma. Axial CT scan shows posterior chest wall invasion (arrow), relative contraindication for Tikhoff-Linberg procedure.

 

Figure 6
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Fig. 4B 33-year-old man with right scapular chondrosarcoma. Anteroposterior conventional radiograph shows limb-sparing surgery, resecting involved part of chest wall along with proximal humerus, distal clavicle, and entire scapula and replacing it with total shoulder prosthesis (Scapular Implant, version 1.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]). This patient had not experienced recurrence at 12-month follow-up.

 
Reconstruction and Implant Types
Multiple reconstructive techniques have been attempted in efforts to stabilize the upper extremity after the Tikhoff-Linberg procedure. Early attempts at preventing a flail upper extremity included various versions of a humeral intramedullary rod that was fixed proximally to either the second rib or the remaining clavicle. Although there was success in preserving distal arm function, a variety of problems were noted, including the potential for proximal migration, skin perforation, and mechanical failure, with little restoration of shoulder function [47]. Modern designs have evolved to include humeral and scapular components that fit together to restore normal force vectors, improving function at the shoulder [2, 7, 8]. The rotator cuff muscles, which arise from or insert on the scapula or proximal humerus, are removed en bloc along with the scapula, distal clavicle, and proximal humerus. Extraarticular resection of the glenohumeral joint is, therefore, performed. The portions of the deltoid, biceps, triceps, coracobrachialis, pectoralis, latissimus dorsi, teres major, serratus anterior, trapezius, and rhomboids that insert on the resected bones are taken down for later use in stabilizing the prostheses. If portions of these muscles are involved with tumor, they are resected as well.

The scapular component of the prosthesis, although anatomically smaller than the human scapula, is created to mimic the normal 40–45° of anteversion of the glenoid cavity with respect to the coronal plane of the body to restore the normal range of motion (Figs. 5A and 5B). This represents the second version of the scapular implant. The scapular implant used in the first several patients in this series had a glenoid cavity that faced laterally, without any anteversion. The proximal humeral implant first had a modular design, with three standardized components that could be mixed and matched to fit any patient (Figs. 6A and 6B). Complications with this version (discussed later) led to the practice of custom-designing a humeral component for each patient.


Figure 7
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Fig. 5A 29-year-old woman with Ewing sarcoma of right scapula. Intraoperative photograph shows size difference between resected scapula and implant (Scapular Implant, version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]) that will replace it. Also note anteversion of glenoid cavity in both resected specimen (arrow) and implant.

 

Figure 8
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Fig. 5B 29-year-old woman with Ewing sarcoma of right scapula. Intraoperative photograph shows implant (Scapular Implant, version 2.0, Nonmodular Humeral Implant) sewn to posterior chest musculature.

 

Figure 10
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Fig. 6A 63-year-old man after Tikhoff-Linberg procedure and total shoulder prosthetic reconstruction for metastatic renal cell carcinoma of scapula. Photograph shows modular version of humeral endoprostheses (Scapular Implant, version 1.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]), consisting of proximal humeral segment (1), intercalary segment (2), and intramedullary component (3).

 

Figure 11
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Fig. 6B 63-year-old man after Tikhoff-Linberg procedure and total shoulder prosthetic reconstruction for metastatic renal cell carcinoma of scapula. Anteroposterior radiograph shows modular humeral implant in place along with scapular implant (Scapular Implant, version 1.0, Modular Humeral Implant).

 
The scapular prosthesis is sutured to the musculature of the chest wall and, usually, the remaining serratus anterior through multiple fenestrations along its borders. Depending on the extent of the remaining muscles, they are sutured to each other and to the implant in a manner that will help restore their normal function and to completely cover the implant. Ideally, the biceps and coracobrachialis may be sutured together and reattached to the remaining clavicle, and the pectoralis major is closed over the new glenohumeral joint. Posteriorly, the levator scapulae, trapezius, rhomboids, and deltoid may be sutured to each other and to the prosthesis [1]. At times, latissimus dorsi flaps may be used to help completely cover the implant.

The total shoulder prosthesis could be categorized as a "constrained" device in that the head of the humeral implant locks into the glenoid cavity of the scapular component. The locking mechanism serves to restore the normal force vectors of the shoulder previously enforced by the rotator cuff muscles, which served to counteract the upward force exerted on the humeral head by the deltoid muscle. Abduction is therefore achieved without upward migration of the humeral head, seen in nonconstrained models [1].

Postoperative Imaging Studies
Baseline imaging—Baseline postoperative conventional radiography studies are usually obtained within 1 week of surgery. These studies consist of chest radiography and anteroposterior scapula, transscapular oblique, and anteroposterior internal–external rotation radiography of the humerus. Baseline studies serve as a benchmark for comparison for all future imaging studies.

Normal findings include the humeral implant in anatomic position with the scapular implant sitting flush against the posterior chest wall. Scapular and humeral components should show no signs of dislocation, and there should be no periprosthetic humeral fracture (Figs. 7A and 7B). MDCT should be included in the diagnostic workup of complex periprosthetic fractures. The chest radiograph is also scrutinized for possible pneumothorax.


Figure 12
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Fig. 7A 19-year-old man after Tikhoff-Linberg procedure and total shoulder prosthetic reconstruction for Ewing sarcoma of left scapula. Anteroposterior internal rotation radiograph shows implant (Scapular Implant, version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]) in good anatomic position with no dislocation or periprosthetic fracture present.

 

Figure 13
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Fig. 7B 19-year-old man after Tikhoff-Linberg procedure and total shoulder prosthetic reconstruction for Ewing sarcoma of left scapula. Transscapular oblique radiograph shows scapular implant body sitting flush against posterior chest wall.

 
Follow-up imaging—Follow-up conventional radiography studies are obtained with protocol and positioning similar to baseline studies. Hardware alignment and positioning should remain stable and unchanged from the baseline studies. A variety of common complications may be encountered and diagnosed with conventional radiography. In addition, follow-up CT examination of the chest is performed to evaluate for lung metastases. Although these studies are not optimal for evaluation of the shoulder, abnormalities and postoperative complications may still be encountered.

Perioperative complications in our series included: three (23%) dislocations (two scapular, one modular humeral), two (15%) local recurrences, one (8%) distant (nonpulmonary) metastasis, and two (15%) lung metastases. Other complications included three (23%) wound seromas and two (15%) incidents of poor wound healing. Three patients have since died of recurrent or metastatic disease.

As shown, dislocation (23%) and disease recurrence (38% overall including local, distant nonpulmonary metastases, and pulmonary metastases) were the most common complications. Dislocations occurred between the components of the modular humeral implant (Figs. 8A, 8B, and 8C) as well as between the humeral head and the scapular glenoid (Fig. 9). Asavamongkolkul et al. [9] reported upward humeral head migration at a rate of 7%. Two (15%) patients in our series required revision surgeries secondary to dislocations.


Figure 14
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Fig. 8A 63-year-old man with metastatic renal cell carcinoma of scapula. Lateral chest radiograph shows dislocation between intercalary (2) and intramedullary (3) components of modular humeral implant (1) (Scapular Implant, version 1.0, Modular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]).

 

Figure 15
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Fig. 8B 63-year-old man with metastatic renal cell carcinoma of scapula. Photograph shows manner in which surgeon reinforced modular humeral model.

 

Figure 16
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Fig. 8C 63-year-old man with metastatic renal cell carcinoma of scapula. Lateral chest radiograph shows reinforced implant in place.

 

Figure 17
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Fig. 9 33-year-old man with right scapular chondrosarcoma after resection and implant placement (Scapular Implant, version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]). Anteroposterior radiograph shows dislocation of humeral head from scapular glenoid.

 
Disease recurrence was seen locally and at distant sites. Rates of local recurrence after limb-sparing surgery are reported to range between 5% and 20% [10, 11]. The local recurrence rate in our series was 15%. Evidence of increased soft-tissue density and rotation or winging of the prosthetic scapula helps with the diagnosis on conventional radiography (Figs. 10A and 10B). Advanced imaging, such as CT and MRI, can delineate recurrent tumor more clearly (Figs. 10C and 10D) and might detect more subtle signs of recurrence such as lymph node enlargement (Figs. 11A, 11B, and 11C).


Figure 18
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Fig. 10A 56-year-old man with left scapular chondrosarcoma after resection and implant placement. (Scapular Implant Version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]). Anteroposterior chest radiograph shows scapular implant in good position immediately after surgery. Also note that postsurgical shoulder lies slightly more inferior in relation to unaffected side, normal postoperative positioning due to small size of scapular implant.

 

Figure 19
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Fig. 10B 56-year-old man with left scapular chondrosarcoma after resection and implant placement. (Scapular Implant Version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]). Anteroposterior chest radiograph 1 year after surgery shows increased axillary soft-tissue density, with loss of muscle planes and scapular implant displaced superiorly and laterally secondary to recurrent tumor. Note that postsurgical shoulder now lies more superior in relation to unaffected limb due to upward pressure from tumor recurrence.

 

Figure 20
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Fig. 10C 56-year-old man with left scapular chondrosarcoma after resection and implant placement. (Scapular Implant Version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]). Coronal STIR image again shows recurrent tumor (black arrows) displacing scapular prosthesis (white arrow) superolaterally.

 

Figure 21
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Fig. 10D 56-year-old man with left scapular chondrosarcoma after resection and implant placement. (Scapular Implant Version 2.0, Nonmodular Humeral Implant; Stryker Orthopaedics [formerly Howmedica Osteonics]). Axial STIR image highlights large, lobulated recurrent tumor (black arrows) laterally displacing scapular implant (white arrow).

 

Figure 22
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Fig. 11A 52-year-old man with right shoulder melanoma recurrence after primary resection and prosthetic placement. Follow-up axial CT scan shows artifact caused by implant (curved arrow) and no significant axillary lymph node enlargement (arrow).

 

Figure 23
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Fig. 11B 52-year-old man with right shoulder melanoma recurrence after primary resection and prosthetic placement. Axial CT scan obtained 3 months after A shows enlarged axillary lymph nodes (arrows), which could represent reactive hyperplasia or recurrent melanoma below level of scapular implant (curved arrow).

 

Figure 24
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Fig. 11C 52-year-old man with right shoulder melanoma recurrence after primary resection and prosthetic placement. Axial MR image shows enlarged and irregular axillary lymph node (arrow). Dark area above lymph node indicated implant (curved arrow).

 
Because total shoulder prosthetic reconstruction is a novel procedure, complication rates have been extrapolated from rates reported for reconstructions using modular spacers or proximal humeral endoprostheses cemented into the remaining humerus. Although proximal humeral endoprostheses are reported in recent studies to show the highest rates of prosthetic survival and the lowest rates of revision and complications [10], some problems may be evident radiologically. The complications (and rates) reported in the literature in the past 10 years include periprosthetic fracture (0–0.7%), deep infection (0–3.4%), and loosening of the humeral prosthesis (0–10.3%) [7, 913]. Most of these complications were not encountered in our series of patients, and illustrations are therefore not included. However, infection and loosening of the humeral stem will share similar findings on conventional radiography, with progressive, abnormally widened interfaces evident between bone and the prosthetic stem. Advanced imaging, nuclear medicine studies, or imaging-guided aspiration of fluid pockets can be used to aid in the differential diagnosis.


Conclusion
Top
Abstract
Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 
Treatment for malignant tumors of the shoulder girdle has evolved radically, with forequarter amputation being much less common today. In addition, when limb-preservation surgery is safe, modern reconstructive efforts try to restore some normal shoulder motion using total shoulder prostheses. Tumors of the scapula or proximal humerus involving the glenohumeral joint but sparing the axillary neurovascular bundle can be considered for Tikhoff-Linberg procedure with total shoulder prosthetic reconstruction. Imaging studies are helpful in identifying patients appropriate for the procedure and recognizing complications postoperatively.


Figure 9
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Fig. 5C 29-year-old woman with Ewing sarcoma of right scapula. Anteroposterior radiograph shows implant (Scapular Implant, version 2.0, Nonmodular Humeral Implant) in place postsurgically.

 


References
Top
Abstract
Introduction
Materials and Methods
Protocols
Results and Discussion
Conclusion
References
 

  1. Malawer MM, Sugarbaker PH, eds. Musculoskeletal cancer surgery: treatment of sarcomas and allied disease. Norwell, MA: Kluwer Academic Publishers, 2001
  2. Malawer MM. Tumors of the shoulder girdle: technique of resection and description of a surgical classification. Orthop Clin North Am 1991; 22:7 -35[Medline]
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  4. Marcove RC, Lewis MM, Huvos AG. En bloc upper humeral interscapulo-thoracic resection: the Tikhoff-Linberg procedure. Clin Orthop Relat Res 1977;124 : 219-228[Medline]
  5. Whitehill R, Wanebo HJ, Mabie KN. Reconstruction after the Tikhoff-Linberg procedure. Arch Surg1982; 117:1248 -1249[Abstract/Free Full Text]
  6. Malawer MM, Sugarbaker PH, Lampert M, Baker AR, Gerber NL. The Tikhoff-Linberg procedure: report of ten patients and presentation of a modified technique for tumors of the proximal humerus. Surgery 1985; 97:518 -528[Medline]
  7. O'Connor M, Sim FH, Chao EYS. Limb salvage for neoplasms of the shoulder girdle: intermediate reconstructive and functional results. J Bone Joint Surg Am 1996;78 : 1872-1878[Abstract/Free Full Text]
  8. Wittig JC, Bickels J, Wodajo F, Kellar-Graney KL, Malawer MM. Constrained total scapula reconstruction after resection of a high-grade sarcoma. Clin Orthop Relat Res 2002;397 : 143-155[CrossRef][Medline]
  9. Asavamongkolkul A, Eckardt JJ, Eilber FR, et al. Endoprosthetic reconstruction for malignant upper extremity tumors. Clin Orthop Relat Res 1999; 360:207 -220[CrossRef][Medline]
  10. Malawer MM, Chou LB. Prosthetic survival and clinical results with use of large-segment replacements in the treatment of high-grade bone sarcomas. J Bone Joint Surg Am 1995;77 : 1154-1165[Abstract/Free Full Text]
  11. Bickels J, Wittig JC, Kollender Y, Kellar-Graney K, Meller I, Malawer MM. Limb-sparing resections of the shoulder girdle. J Am Coll Surg 2002; 348:422 -435
  12. Wittig JC, Bickels J, Kellar-Graney KL, et al. Osteosarcoma of the proximal humerus: long-term results with limb-sparing surgery. Clin Orthop 2002; 397:156 -176[CrossRef][Medline]
  13. Rodl RW, Gosheger G, Gebert C, et al. Reconstruction of the proximal humerus after wide resection of tumours. J Bone Joint Surg Br 2002; 84:1004 -1008[CrossRef][Medline]

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