Overview of Resections around the Shoulder Girdle
BACKGROUND
The upper extremity is involved by bone and soft tissue neoplasms only one-third as often as the lower
extremity.3 The scapula and proximal humerus are common sites of primary sarcoma, including osteosarcoma and Ewing sarcoma in children and chondrosarcoma in adults. Metastatic tumors, especially hypernephroma, also have a propensity for the proximal humerus. When soft tissue tumors occur in the upper extremity, they tend to favor the shoulder girdle and may secondarily involve the scapula, proximal humerus, or clavicle. The axilla is another site around the shoulder girdle where primary soft tissue tumors may develop or where metastases can spread to and replace the local lymph nodes. The axilla is a relatively “silent” area, where tumors may grow to large sizes before they become symptomatic and are detected.
The shoulder girdle consists of the proximal humerus, the scapula, and the distal third of the clavicle as well as the surrounding soft tissues. Each bone may be involved by a primary malignant bone tumor or metastases, with or without soft tissue extension. The bones of the shoulder girdle also may be secondarily involved by a soft tissue sarcoma, which requires resection and reconstruction techniques similar to those of a primary bone tumor (FIG 1).
Until the mid-20th century, forequarter amputation was the treatment for malignant tumors of the shoulder girdle. Today, about 95% of patients with sarcomas of the shoulder girdle can be treated safely by limb-
sparing resection such as the Tikhoff-Linberg resection and its modifications.6 The relation of the neurovascular bundle to the tumor and other structures of the shoulder girdle is the most significant anatomic factor in determining resectability, removal of the tumor, and reconstruction.
The resection and reconstruction of tumors of the shoulder girdle consists of three components:
Surgical resection of the tumor following oncologic principles Reconstruction of the skeletal defect (ie, endoprosthetic replacement)
Soft tissue reconstruction using multiple muscle transfers to cover the skeletal reconstruction and provide a functional extremity
The goals of all shoulder girdle reconstructions are to provide a stable shoulder and to preserve normal elbow and hand function. The extent of tumor resection and remaining motor groups available for reconstruction dictate the degree of shoulder motion and function that are retained.
Historical Background
Some of the earliest discussions concerning limb-sparing surgery focused on techniques for resection of tumors about the scapula. Initial reports of shoulder girdle resections were confined to the individual bones or portions of the scapula. The first reported scapular resection was a partial scapulectomy performed by Liston in 18197 for an ossified aneurysmal tumor. Between this time and the mid-1960s, several other authors
discussed limb-sparing resections about the shoulder girdle.4,11,12,13,14,15,16,19 In 1965, Papioannou and
Francis17 reported 26 scapulectomies and discussed the indications and limitations of the procedure.
The Tikhoff-Linberg interscapulothoracic resection or triple-bone resection was described in the Russian
literature by Baumann1 in 1914. He referred to a 1908 report by Pranishkov that described the removal of the scapula, the head of the humerus, the outer one-third of the clavicle, and the surrounding soft tissue for a sarcoma of the scapula. The shoulder was suspended from the remaining clavicle by metal sutures. Tikhoff and Baumann performed three such operations between 1908 and 1913, and Tikhoff was named as the originator of the procedure. The technique became established in the Western surgical community only after
Linberg's English publication in 1926.6
Classically, most shoulder girdle resections were done for low-grade tumors of the scapula and for periscapular soft tissue sarcomas. Before 1970, most patients with high-grade spindle cell sarcomas (eg, osteosarcoma, chondrosarcoma) involving the shoulder girdle were treated with a forequarter amputation. In
1977, Marcove et al12 were the first to report limb-sparing surgery for high-grade sarcomas arising from the proximal humerus. These authors reported performing an en bloc extra-articular resection that included the proximal humerus, glenoid, overlying rotator cuff, lateral two-thirds of the clavicle, deltoid, coracobrachialis, and proximal biceps. Local tumor control and survival rates were similar to those achieved with a forequarter amputation. Resection, however, preserved a functional hand and elbow. These early results were confirmed
by other surgeons.5,18 After the 1980s, osteosarcoma, chondrosarcoma, and Ewing sarcoma of the proximal humerus became the tumors most commonly treated with a Tikhoff-Linberg resection. A variety of new techniques and modifications of shoulder girdle resections have been developed. Most have been reported as Tikhoff-Linberg or modified Tikhoff-Linberg resections. These eponyms are not accurate descriptions, however, because the Tikhoff-Linberg procedure was not intended to refer to sarcomas of the humerus.
As the popularity of limb-sparing surgery for shoulder girdle sarcomas grew, the extent of resection necessary for various tumors, particularly indications for an extra-articular resection, remained a matter of debate. The best method for reconstruction also came under considerable discussion.
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In response, Malawer et al developed a surgical classification system (FIG 2) based on tumor location, extent, grade, and pathologic type. This system was intended to provide guidelines regarding the extent of resection necessary for primary bone sarcomas and soft tissue sarcomas that secondarily involve the bones of the shoulder girdle.
FIG 1 • Three-dimensional schematic drawing of the shoulder girdle and axillary contents. The brachial plexus and axillary artery and vein are demonstrated coursing through the axillary space. The proximal humerus, clavicle, and scapula are seen here. The musculature of the axillary space forms the borders of the compartment, including the pectoralis major, latissimus dorsi, short head of the biceps, and clavicle. (Courtesy of Martin M. Malawer.)
SURGICAL CLASSIFICATION SYSTEM
The current surgical classification system was described by Malawer and associates2,8,9,10 in 1991 (see FIG 2). It is based on the current concepts of surgical margins, the relation of the tumor to anatomic compartments (ie, intracompartmental vs. extracompartmental), the status of the glenohumeral joint, the magnitude of the individual surgical procedure, and precise considerations of the functionally important soft tissue components. It includes six categories:
Type I: intra-articular proximal humeral resection Type II: partial scapular resection
Type III: intra-articular total scapulectomy
Type IV: extra-articular total scapulectomy and humeral head resection (classic Tikhoff-Linberg resection) Type V: extra-articular humeral and glenoid resection
Type VI: extra-articular humeral and total scapular resection
Each type is subdivided according to the status of the abductor mechanism (the deltoid muscle and rotator cuff):
Abductors intact
Abductors partially or completely resected
Type A resections, in which the abductors are preserved, usually are recommended for high-grade spindle cell bone sarcomas that are entirely intracompartmental (ie, contained within either the proximal humerus or scapula bone). This is a rare situation, however. This type of resection also is recommended for low-grade bone sarcomas, selected metastatic carcinomas, and, often, round cell sarcomas.
Type B resections, in which the abductors are resected, are extracompartmental resections and are the most common type of resection performed for high-grade spindle cell sarcomas.
All six of these types of shoulder girdle resections and their indications are described briefly in the following section. The surgical techniques for each resection and reconstruction are described in Chapters 9, 10, and 11,12 and 13 in this section.
GUIDELINES FOR SHOULDER GIRDLE RESECTION
Local Growth and Transarticular Involvement by Shoulder Girdle Tumors
The shoulder joint appears to be more prone than other joints to intra-articular or pericapsular (ligamentous) involvement by high-grade bone sarcomas.
Four basic mechanisms underlie tumor spread across the shoulder joint: direct capsular extension, tumor extension along the long head of the biceps tendon, fracture hematoma from a pathologic fracture, and poorly planned biopsy (FIG 3).
These mechanisms place patients undergoing intra-articular resections for high-grade sarcomas at greater risk for local recurrence than those undergoing extra-articular resections. Therefore, it often is necessary to perform an extra-articular resection for high-grade bone sarcomas of the proximal humerus or scapula.
Most tumors arise from the metaphyseal portion of the proximal humerus. They extend beyond the cortices and spread underneath the deltoid muscle, subscapularis muscle, and remaining rotator cuff muscles. As the tumor grows, the extraosseous component spreads along the long head of the biceps tendon, along the glenohumeral ligaments, and underneath the rotator cuff, heading toward the glenoid or directly crossing the glenohumeral joint. The deltoid, subscapularis, and remaining rotator cuff muscles are compressed into a pseudocapsular layer. These muscles form compartmental boundaries around the tumor. The axillary nerve and circumflex vessels enter this compartment. The major neurovascular bundle is displaced by the tumor; however, in most instances, the fascia overlying the subscapularis muscle as well as the axillary sheath that contains the blood vessels and nerves protect the major neurovascular bundle from tumor involvement or encasement.
Similarly, most scapular sarcomas originate from the metaphyseal portion of the scapula or the scapula neck and grow centripetally into the soft tissues. They form a soft tissue mass that extends outward and usually is contained by the subscapularis and other rotator cuff muscles. These tumors follow the path of least resistance and are directed toward the glenohumeral joint and proximal humerus. Eventually, the tumor
contaminates these structures. The subscapularis muscle and its investing fascia function as a barrier and protect the axillary vessels and brachial plexus from tumor invasion. These neurovascular structures usually are displaced by the adjacent tumor that lies deep to the subscapularis muscle.
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FIG 2 • Classification of shoulder girdle resections as reported by Malawer in 1991. (Reprinted with permission from Malawer MM, Meller I, Dunham WK. A new surgical classification system for shoulder-girdle resections.
Analysis of 38 patients. Clin Orthop Relat Res 1991;267:33-44.)
Functional Anatomic Compartment of the Shoulder Girdle
Sarcomas grow locally in a centripetal manner and compress surrounding tissues (muscles) into a pseudocapsular layer. The pseudocapsular layer contains microscopic fingerlike projections of tumor, which are referred to as satellite nodules.
FIG 3 • Biopsy site. Anatomic drawing illustrating the preference for a core needle biopsy for tumors of the proximal humerus. The biopsy sample should betaken through the anterior third of the deltoid. Great care should be taken to avoid the pectoralis major muscle, the deltopectoral interval, and the axillary vessels. The deltoid is innervated by the axillary nerve posteriorly, so a portion of the anterior deltoid can be resected if necessary without significant compromise to the nerve. (Courtesy of Martin M. Malawer. From Bickels J, Jellnek S, Shmookler BM, et al. Biopsy of musculoskeletal tumors. Current concepts. Clin Orthop Relat Res 1999;368:212-219.)
Sarcomas spread locally along the path of least resistance. Surrounding fascial layers resist tumor penetration and, therefore, provide boundaries to local sarcoma growth. These boundaries form a compartment around the tumor (FIG 4).
A sarcoma will grow to fill the compartment in which it arises, and only rarely will an extremely large sarcoma
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extend beyond its compartmental borders. In discussing bony sarcomas that extend beyond the cortices into the surrounding soft tissues, the term functional anatomic compartment refers to the investing muscles that are compressed into a pseudocapsular layer (see FIG 4).
FIG 4 • Schematic diagram of the compartment of the proximal humerus. A true compartmental site includes the muscles of origin and insertion of a specific group as well as a major feeding vessel and nerve. This is a conceptual consideration for tumors around the proximal humerus, which does not fit the classic definition of an anatomic compartment. Surgically, however, this area is considered as the shoulder girdle compartment, which consists of the deltoid, the rotator cuff muscles, a portion of the pectoralis major muscle, the latissimus dorsi, and the teres major. The major neurovascular pedicle is the axillary nerve and the circumflex vessels. (Courtesy of Martin M. Malawer. From Wittig JC, Bickels J, Kellar-Graney KL, et al. Osteosarcoma of the proximal humerus: long-term results with limb-sparing surgery. Clin Orthop Relat Res 2002;[397]:156-176.)
These muscles provide the fascial borders of the compartment, a fact that has important surgical implications. A wide resection of a bone sarcoma removes the entire tumor and pseudocapsular layer and must, therefore, encompass the investing muscle layers (compartmental resection).
The functional compartment surrounding the proximal humerus consists of the deltoid, subscapularis, and remaining rotator cuff, latissimus dorsi (more distally), brachialis, and portions of the triceps muscles. The glenoid and scapular neck also reside within the functional compartment of the proximal humerus because they are contained by the rotator cuff and capsule and the subscapularis muscle. Sarcomas that arise from the proximal humerus and extend beyond the cortices compress these muscles into a pseudocapsular layer.
The fascial layers surrounding these muscles resist tumor penetration. The only neurovascular structures that enter this compartment are the axillary nerve and humeral circumflex vessels.
The main neurovascular bundle (ie, brachial plexus and axillary vessels) to the upper extremity passes anterior to the subscapularis and latissimus dorsi muscles. These muscles and their investing fascial layers are particularly important, therefore, for protecting the neurovascular bundle from tumor involvement. They also protect the pectoralis major muscle, which must be preserved during surgical resection for soft tissue coverage.
High-grade sarcomas that extend beyond the bony cortices of the proximal humerus expand the investing
muscles that form the compartmental borders and pseudocapsular layer.
These sarcomas grow along the path of least resistance and, therefore, are directed toward the glenoid and scapular neck by the rotator cuff and glenohumeral joint capsule.
Anteriorly, the tumor is covered by the subscapularis, which bulges into and displaces the neurovascular bundle. Only rarely does a very large proximal humerus sarcoma extend beyond the compartmental borders.
In these instances, the tumor usually protrudes through the rotator interval. A wide (compartmental) resection for a high-grade sarcoma must, therefore, include the surrounding muscles that form the pseudocapsular layer (ie, deltoid, lateral portions of the rotator cuff), the axillary nerve, humeral circumflex vessels, and the glenoid (extra-articular resection of the proximal humerus).
Most high-grade scapular sarcomas arise from the region of the scapular neck. The compartmental borders surrounding the scapular neck consist of the rotator cuff muscles and portions of the teres major and latissimus dorsi muscles. The compartment consists of all of the muscles that originate on the anterior and posterior surfaces of the scapula: the subscapularis, infraspinatus, and teres muscles. The deltoid, although it is not typically considered one of the compartmental borders because it attaches to a narrow region of the scapular spine and acromion, may be involved secondarily by a large soft tissue extension. In most instances, the deltoid is protected by the rotator cuff muscles because the anatomic origin of most tumors is from the neck and body region. Similar to the proximal humerus, the rotator cuff muscles are compressed into a pseudocapsular layer by sarcomas that arise from the scapula. The subscapularis also protects the neurovascular bundle from tumor involvement. The head of the proximal humerus is contained within the compartment surrounding the scapula by the rotator cuff muscles. Wide resection of a high-grade scapular sarcoma must, therefore, include the rotator cuff and, in most instances, the humeral head.
The axillary nerve is not contained within the compartment and therefore can be spared from resection. Additionally, because the deltoid is not compressed into a pseudocapsular layer, it usually can be preserved.
INDICATIONS
Indications for Limb Sparing Surgery
Selection of patients for limb-sparing surgery is based on the anatomic location of the tumor and a thorough understanding of the natural history of sarcomas and other malignancies:
High-grade and some low-grade bone sarcomas Soft tissue sarcomas arising from the shoulder girdle
Metastatic carcinomas: isolated metastasis or metastatic lesions that have caused significant bony destruction
Occasionally, benign aggressive tumors also may require these treatment techniques.
Contraindications for Limb Sparing Surgery
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Absolute contraindications for limb-sparing procedures include tumor involvement of the neurovascular bundle or a patient's inability or unwillingness to tolerate a limb-sparing operation.
Relative contraindications may include chest wall extension; pathologic fracture around the shoulder girdle; previous infection; lymph node involvement; or a complicated, inappropriately placed biopsy that has resulted in extensive hematoma, which has resulted in tissue contamination.
Biopsy Site
One of the most common causes for forequarter amputation is an inappropriately placed biopsy site that has resulted in contamination of the pectoralis muscles, neurovascular structures, and chest wall.
Extreme care must be taken with biopsy placement and technique (see FIG 3).
Vascular Involvement
Fortunately, most tumors of the proximal humerus are separated from the anterior vessels by the subscapularis, latissimus dorsi, and coracobrachialis muscles. It is rare for the axillary or brachial artery to be involved with tumor, although a large soft tissue component may cause displacement and compression.
In general, if the vessels appear to be involved with tumor, the adjacent brachial plexus also is involved, and a limbsparing procedure may be contraindicated.
Nerve Involvement
The three major cords of the brachial plexus follow the artery and vein and rarely are involved with tumor. The axillary nerve may be involved by neoplasm as it passes from anterior to posterior along the inferior glenohumeral joint capsule. Resection of the axillary nerve usually is required for stage IIB tumors of the proximal humerus.
The musculocutaneous and radial nerves rarely are involved. The deficit created by resecting the radial nerve is greater than that for the musculocutaneous nerve, but this should not be an indication for amputation.
If resection will lead to a major functional loss and a close margin (increasing the risk of local recurrence), amputation should be considered. Direct tumor extension into or encasement of the brachial plexus necessitates a forequarter amputation.
Lymph Nodes
Bone sarcomas rarely involve adjacent lymph nodes; nevertheless, axillary nodes should be evaluated and may require biopsy. In the rare incidence of lymph node involvement documented by biopsy, a forequarter amputation may be the best method for removing all gross disease.
Alternatively, a lymph node dissection in conjunction with a limb-sparing procedure may be considered. Malawer (unpublished data, 2009) has found, based on two cases, that local control and long-term survival can be obtained by this method.
Chest Wall Involvement
Tumors of the shoulder girdle with large extraosseous components occasionally may involve the chest wall, ribs, and intercostal muscles.
Chest wall involvement should be evaluated preoperatively with physical examination and imaging studies; however, such involvement often is not determined until the time of surgery. It is not an absolute indication for forequarter amputation; a limb-sparing procedure combined with a chest wall resection may be performed, depending on the involvement of adjacent soft tissues and neurovascular structures.
Previous Resection
The local recurrence rate is increased in cases in which a wide resection is attempted (1) following a previous inadequate resection around the shoulder girdle or (2) when a tumor already has recurred locally. This possibility must be a consideration especially with tumors of the scapula and clavicle and of soft tissue tumors that involve the proximal humerus.
Infection
In patients with high-grade sarcomas, limb-sparing procedures performed in an area of infection are
extremely risky because these patients must receive postoperative adjuvant chemotherapy. If an infection cannot be eradicated with the primary resection, amputation is advisable.
SURGICAL MANAGEMENT
Preoperative Planning
Physical Examination
The physical examination is essential for assessing tumor resectability and for estimating the extent of resection that may be required. Physical examination is important in determining tumor extension into the glenohumeral joint, neurovascular involvement, or tumor invasion of the chest wall. If tumor has invaded the joint, shoulder range of motion usually is reduced, and the patient may complain about discomfort and pain.
Neurovascular involvement or compression may be suggested by an abnormal neurologic examination or by decreased or absent pulses. Distal edema in the upper extremity means a probable tumoral infiltration in neurovascular structures.
Tumors that move freely with respect to the chest wall usually are separated from it by at least a thin tissue plane through which it is safe to dissect.
Determining Tumor Resectability
High-grade tumors arising from the shoulder girdle region often are large and encroach on the neurovascular bundle. Tumors that encase or invade the brachial plexus are considered unresectable. In many cases, it is difficult to determine, both clinically and radiologically, which tumors involve or encase the neurovascular structures directly as opposed to merely displacing these structures. Although most tumors that displace the neurovascular structures are resectable, some are unresectable, and it can be difficult to determine clinically which are in this category.
We have found the clinical triad of intractable pain, motor deficit, and a venogram showing obliteration of the axillary vein to be very reliable in predicting brachial plexus invasion. No single imaging study is available that accurately visualizes the brachial plexus. Magnetic resonance imaging (MRI) and computed tomography (CT) scans typically show a large tumor juxtaposed to the neurovascular bundle (FIG 5).
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FIG 5 • Imaging studies of the shoulder girdle and axillary space demonstrating bony and soft tissue findings.
A. CT scan showing a tumor arising from the glenoid and involving the glenohumeral joint. CT scans are the best modality for observing bony detail. B. Coronal MRI scan showing direct tumor extension. C,D. A large soft tissue axillary tumor (arrows) protruding anteriorly through the pectoralis major and the skin. This is a high-grade fungating soft tissue sarcoma. MRI is the best scan for evaluation of soft tissue masses in relation to other soft tissue structures. E. MRI scan of the axillary space (coronal view) showing a secondary skipped lesion along the axillary vein, coming from a high-grade soft tissue sarcoma lower in the axilla. Metastatic lesions of the axilla and lymph nodes are a common source of large axillary masses and are best evaluated by MRI scans. F. Angiography and embolization of metastatic renal cell carcinoma (hypernephroma) to the distal clavicle. Following embolization, there is no evidence of a tumor blush. Embolization often is performed for large high-grade soft tissue sarcomas prior to a resection. (continued)
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FIG 5 • (continued) G. On this axillary venogram, the axillary vein is occluded by thrombosis, and there is a small backward filling from the innominate vein. This is the most pathognomonic finding of brachial plexus involvement seen during the time of surgery. Brachial plexus involvement often correlates with the clinical findings of neurologic deficits, numbness, or muscle weakness of the affected extremity. H. Three-dimensional angiogram demonstrating the arteries of the shoulder girdle. Angiograms are particularly useful in determining patency of the vessels and local anatomy or anatomic anomalies within the surgical field as well as angiogenesis to particularly vascular tumors.
Venography, however, is extremely accurate in predicting brachial plexus invasion. The axillary vein, axillary artery, and brachial plexus travel in intimate association within a single fascial sheath, the axillary sheath.
The major nerves and cords travel along the periphery of the sheath; therefore only complete obliteration—not just compression—of the brachial or axillary vein denotes direct tumor extension in and around the nerves and also indicates secondary involvement of the venous wall. This progression also explains the clinical triad of pain, motor loss, and venous obstruction.
Tumors that invade or encase the brachial plexus obliterate the axillary vein because of that vein's thin walls and low intraluminal pressure. In these instances, arteriography demonstrates displacement of the axillary artery; however, the axillary artery remains patent because of its thick walls and high intraluminal pressures.
The final decision regarding the need for a forequarter amputation should be reserved until surgical exploration of the brachial plexus has been performed.
Prosthetic Reconstruction
When endoprosthetic reconstruction was developed in the 1940s, attention initially was focused on reconstruction of skeletal defects of the lower extremity. Use of the technique was broadened gradually to include defects of the upper extremity and shoulder girdle.
The Modular Replacement System (MRS) shoulder prosthesis has undergone several design changes and improvements since that time. The current components for proximal humerus and scapular replacement are shown in Chapters 9 and 10, respectively. The MRS is used in conjunction with both intra- and extra-articular resections, and results are highly predictable and successful.
Reported rates of fracture, infection, nonunion, reoperation, and tumor recurrence are lower, and length of immobilization is shorter with extremity endoprosthetic reconstruction than with allograft, composite reconstruction, or arthrodesis.
Survival of the MRS proximal humeral prosthesis is reported to be 95% to 100% at 10 years.
TECHNIQUES
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Skeletal Reconstruction following Humerus and Scapular Resections
Special prosthetic replacements are recommended for skeletal reconstruction following proximal humerus and total scapular resections, although the utilitarian approach may be used with any method of reconstruction (TECH FIG 1).
Soft tissue reconstruction is accomplished using a dual suspension technique that employs static and dynamic methods of prosthetic stabilization and soft tissue and motor reconstruction.
Static methods of stabilization include the use of heavy nonabsorbable sutures, Dacron tapes, or Gore-Tex grafts, depending on the site of tumor resection and the prosthesis that is being used. This method offers secure fixation and stabilization of the prosthesis until the soft tissues heal and scar to each other.
Dynamic methods of stabilization and reconstruction include multiple muscle rotation flaps and muscle transfers that eventually heal, scar to each other and the prosthesis, and provide the necessary motor units for a functional extremity.
Soft tissue reconstruction follows skeletal reconstruction and static stabilization. The short head of the biceps is attached with a tenodesis proximally to the coracoid (intra-articular proximal humerus reconstruction), the clavicle (extra-articular proximal humerus reconstruction), or pectoralis major (total scapula reconstruction). The pectoralis minor also is tenodesed back to its origin, when possible, or to the scapula to protect the neurovascular structures. The pectoralis major is repaired to its humeral insertion or, in
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cases requiring extra-articular proximal humerus reconstruction, transferred to cover the prosthesis with soft tissues. The latissimus dorsi may be transferred laterally to function as an external rotator following extra-articular proximal humerus resection.
TECH FIG 1 • A. Utilitarian incision. This incision has been developed based on the extensive experience of surgeons performing resections around the shoulder girdle. It consists of three components. Dashed line A indicates the anterior approach, an extended deltopectoral incision coming from the midclavicle through the deltopectoral interval and distally over the medial aspect of the arm, curving in a posterior direction. Dashed line B is a posterior incision that is somewhat curved in nature to allow development of a large posterior fasciocutaneous flap for exposure of the entire scapula and rhomboid region. Dashed line C is an incision that connects A and B through the axillary folds. This permits resection of large axillary tumors or performance of forequarter amputations. B. The initial steps of the anterior approach of the utilitarian shoulder girdle incision. The key to this approach is the release of the pectoralis major from its insertion on the humerus (1 to 2 cm away). With the pectoralis major now reflected onto the chest wall, the entire axillary space can be exposed. This is termed the first layer of musculature of the axillary space. The second muscular layer of the axillary space is then visualized. With the pectoralis major layer retracted, the axillary space is completely covered by fascia, similar to the peritoneum. This covers two muscles, the short head of the biceps and the pectoralis minor, which attach to the coracoid process, which must be released. With these two muscles released, the axillary space and infraclavicular
component of the brachial plexus (ie, the axillary vein and artery through its entire length) can be explored completely. If necessary, a portion of the clavicle can be resected to expose the subclavian artery and vein. (continued)
TECH FIG 1 • (continued) C. Intraoperative photograph demonstrating the axillary exposure following the utilitarian shoulder girdle incision. Once the pectoralis major and deltoid muscles have been retracted, the infraclavicular component of the axillary vessels can be visualized. The biopsy tract will be removed in situ to prevent contamination of the compartment. (Courtesy of Martin M. Malawer.)
In total scapula reconstruction, the periscapular muscles are tenodesed to the prosthesis with heavy nonabsorbable sutures or tapes in a manner that covers the entire prosthesis with muscle. Following isolated axillary tumor resection, the distal (humeral) transected edge of the latissimus dorsi muscle is rotated into the defect and sutured to the superficial surface of the subscapularis muscle to fill the dead space. Large-bore closed suction drains are routinely placed prior to skin closure.
PEARLS AND PITFALLS
Preoperative
evaluation
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Physical examination and radiologic imaging modalities are useful for predicting whether a tumor is resectable. The
scapula and proximal humerus should move freely from the chest wall. Chronic swelling in the distal extremity, intractable pain, motor loss, and a venogram that demonstrates obliteration of the axillary vein strongly suggest that the tumor is
unresectable. The final determination regarding the need for a forequarter amputation is made intraoperatively, after anterior
exposure and exploration of the brachial plexus and neurovascular structures.
Neurovascular
exploration and mobilization
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The key to a safe and adequate resection of all types of neoplasms around the shoulder girdle lies in adequate
visualization, exposure, dissection, mobilization, and preservation of all vital neurovascular structures. Full exposure is facilitated by releasing the pectoralis major muscle from its humoral insertion and the strap muscle from the coracoid process.
Type of
resection
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High-grade sarcomas that arise from the proximal humerus or scapula are likely to contaminate or cross the glenohumeral
joint, either grossly or microscopically. An extra-articular type of resection is used for most high-grade sarcomas arising from the scapula or proximal humerus. Clavicular tumors, although less common, require a slightly different surgical approach (FIG 6).
Soft tissue
reconstruction
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Soft tissue reconstruction is just as important as skeletal reconstruction during limb-sparing surgery if a functional
extremity is to be provided. Static and dynamic methods of soft tissue reconstruction and stabilization are used. Static methods rely on heavy nonabsorbable sutures, Dacron tapes, and Gore-Tex grafts. Dynamic methods rely on multiple muscle transfers and rotational muscle flaps.
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FIG 6 • Example of a safe exposure of a clavicular tumor. The tumor arising from the distal clavicle is a solitary metastasis. The trapezius has been mobilized. The pectoralis major has been detached from the clavicle, and the deltoid has been detached from the acromion.
FIG 7 • A. Results of 134 shoulder girdle resections classified as type of resection versus function as measured by the Musculoskeletal Tumor Society (MSTS) scale. B. Composite photograph demonstrating head, body, and stem components for humeral resections. C. Proximal humerus modular replacement system options from Stryker Orthopaedics. D. Proximal humerus and scapular prosthesis system. E. Plain radiograph following reconstruction using a constrained total scapula replacement.
OUTCOMES
The types of tumors, anatomic locations, and types of shoulder girdle resections performed in 134 patients treated at the authors' institutions from 1980 to 1998 are shown in FIG 7A. Experience in these patients with endoprosthetic reconstruction of the proximal humerus and scapula demonstrates that this is a reliable and durable technique of reconstruction (FIG 7B-E).
In the same publication, the function after the surgery was estimated to be good to excellent in 101 patients (75.4%), moderate in 23 patients (17.1%), and poor in 10 patients (7.5%).
Overall, patients with intra-articular resection and reconstruction have better functional outcomes than patients who underwent extra-articular resections and reconstruction.
Survival rates based on Kaplan-Meier analysis demonstrate a 9-year survival rate of 98% to 99% for proximal humeral replacements.
No mechanical failures or dislocations occurred. Other groups have reported a significant incidence of dislocation following endoprosthetic reconstruction of the shoulder girdle, but this has not been our experience, attributable to the soft tissue reconstruction.
The results shown in FIG 7A reflect the use of “dual suspension” (ie, both static and dynamic) or capsular reconstruction techniques and meticulous attention to soft tissue reconstruction.
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FIG 8 • Clinical photograph of a patient 2 years postoperatively demonstrating the anterior incision scar as well as a custom right shoulder orthosis. She is able to wear regular undergarments with the use of the orthosis and has an approximately anatomic contour to the shoulder.
Normal hand dexterity and complete range of motion of the elbow is expected after limb-sparing surgery of the shoulder girdle.
Good cosmetic appearance is gained through the use of a custom shoulder orthosis (FIG 8).
COMPLICATIONS
The utilitarian shoulder approach ensures safe mobilization of major neurovascular structures. Optimal surgical margins are facilitated, and unnecessary complications and local recurrences are minimized.
Nerve complications after shoulder girdle resection can occur rarely but are transient.
Typically, they occur as a result of nerve traction during surgery or secondary to the immediate postoperative swelling. Normally, 6 months after the surgery, all nerve palsies were resolved.
Wound infection is described in approximately 2.5% of the patients who were treated with limb-sparing surgery.
REFERENCES
-
Baumann PK. Resection of the upper extremity in the region of the shoulder joint. Khirurgh Arkh
Velyaminova 1914;30:145.
-
Bickels J, Wittig JC, Kollander Y, et al. Limb-sparing resection of the shoulder girdle. J Am Coll Surg 2002;194(4):422-435.
-
Dahlin DC. Bone Tumors: General Aspects and Data on 6,221 Cases, ed 3. Springfield, IL: Charles C Thomas, 1978.
-
Francis KC, Worcester JN. Radical resection for tumors of the shoulder with preservation of a functional extremity. J Bone Joint Surg Am 1962;44A:1423-1430.
-
Guerra A, Capanna R, Biagini R, et al. Extra-articular resection of the shoulder (Tikhoff-Linberg). Ital J Orthop Traumatol 1985; 11:151-157.
-
Henshaw RM, Jones V, Malawer MM. Endoprosthetic replacement with the modular replacement system: survival analysis of the first 100 implants with a minimum 2-year follow-up. Presented at the Combined Meeting of the American and European Musculoskeletal Tumor Societies, May 6-10, 1998, Washington, DC.
-
Linberg BE. Interscapulo-thoracic resection for malignant tumors of the shoulder girdle region. J Bone Joint Surg 1928;10:344.
-
Liston R. Ossified aneurysmal tumor of the subscapular artery. Eduil Med J 1820;16:66-70.
-
Malawer MM. Tumors of the shoulder girdle: technique of resection and description of a surgical classification. Orthop Clin N Am 1991;22:7-35.
-
Malawer MM, Link M, Donaldson S. Sarcomas of bone. In: DeVita VT, Hellman S, Rosenberg SA, eds. Cancer: Principles and Practice of Oncology, ed 3. Philadelphia: JB Lippincott, 1984:1418-1468.
-
Malawer MM, Sugarbaker PH, Lambert MH, et al. The Tikhoff-Linberg procedure and its modifications. In: Sugarbaker PH, ed. Atlas of Sarcoma Surgery. Philadelphia: JB Lippincott, 1984.
-
Marcove RC. Neoplasms of the shoulder girdle. Orthop Clin N Am 1975;6:541-552.
-
Marcove RC, Lewis MM, Huvos AG. En-bloc upper humeral interscapulothoracic resection. The Tikhoff-Linberg procedure. Clin Orthop 1977;124:219-228.
-
Mussey RD. Removal by dissection of the entire shoulder blade and collar bone. Am J Med Sci 1837;21:390-394.
-
Pack GT, Baldwin JC. The Tikhoff-Linberg resection of the shoulder girdle. Case report. Surgery 1955;38:755-757.
-
Pack GT, Crampton RS. The Tikhoff-Linberg resection of the shoulder girdle. Clin Orthop 1961;19:148-161.
-
Papioannou AN, Francis KC. Scapulectomy for the treatment of primary malignant tumors of the scapula. Clin Orthop 1965;41:125.
-
Rosenberg SA, Suit FD, Baker LH. Sarcomas of soft tissue. In: Devita VT, Hellman S, Rosenberg SA, eds. Cancer: Principles and Practice of Oncology, ed 2. Philadelphia: JB Lippincott; 1985:1243-1293.
-
Samilson RL, Morris JM, Thompson RW. Tumors of the scapula: a review of the literature and an analysis of 31 cases. Clin Orthop 1968;58:105-115.
-
Syme J. Excision of the Scapula. Edinburgh: Edmonston and Douglas, 1864.
-
Wittig JC, Bickels J, Wodajo F, et al. Utilitarian shoulder approach for malignant tumor resection. Orthopedics 2002;5:479-484.