Plexo Braquial Transmanubrial Transclavicular Approach in Tumors of the Brachial Plexus.

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Authors: García-López A, Iborra A.

Abstract: The standard transclavicular approach allows only limited and narrow exposure if the cervical thoracic region for the resection of tumors of the brachial plexus is involved. We report 2 cases of retroclavicular tumors of the brachial plexus. We performed a complete resection in both cases using the transmanubrial transclavicular approach. This approach consists of retracting an osteomuscular flap that involves the medial portion of the clavicle, part of the sternal manubrium, the sternoclavicular joint, and the sternocleidomastoid muscle. We describe and discuss this approach, whichprovides access to the entire brachial plexus and the major vessels, thereby affording excellent control of the vessels; it is the approach of choice for tumors in this location.

Key Words: brachial plexus, connective and soft tissue neoplasms, limb
salvage, paralysis, wound closure techniques
(Ann Plast Surg 2011;67: 387–390)

Tumors of the brachial plexus are difficult to remove, as they involve neural or vascular structures and because of their deep location. Retroclavicular tumors are particularly complex because they also involve the neural structures of the brachial plexus itself, the phrenic and vagus nerves (X), the recurrent laryngeal nerve, the supra-aortic arterial trunks and their branches, the brachiocephalic venous trunks, the chest wall, and the thoracic duct on the left side.

They may extend toward the supraclavicular or infraclavicular region, toward the mediastinum, or the axillary region. Tumor resection that spares the limb is the initial objective of our approach to these tumors located in the area of the cervicothoracic transition.

An approach is required that allows us to fully expose the entire plexus with medial extension toward the origin of the subclavian and carotid vessels, the apex, and chest wall, and the possibility to extend to the axilla.

We report 2 cases of tumors of different types and behavior, in similar locations, and discuss their resection using the transclavicular trans-sternal approach. We describe and discuss this approach, which affords suitable exposure and control of the branching of the brachycephalic vein into the external and internal jugular veins, and the subclavian vein, the most proximal section of the subclavian artery, the vertebral artery, and the recurrent laryngeal
nerve.

CASE REPORTS

Case 1

The patient was an 8-year-old boy whose first symptom was pain in the shoulder after swimming. The patient visited another hospital, after a lump was felt in the left supraclavicular fossa; magnetic resonance imaging (MRI) revealed a tumor affecting the left brachial plexus and the subclavian artery and vein. An incisional
biopsy was performed, leading to postoperative partial loss of feeling in the first and second fingers of the hand. The biopsy results revealed aggressive myofibromatosis and the patient visited several surgical departments that ruled out resection; chemotherapy was therefore instated by the oncology department with methotrexate and vinorelbine.

The patient was referred to our brachial plexus surgery unit for evaluation 5 months after diagnosis. Physical examination revealed a 7-cm horizontal supraclavicular lesion parallel to the clavicle, under which was a hard mass that was strongly adhered to the deep layers. The strength of his pectoralis major, biceps brachii, and brachialis muscles was grade 4 on the Medical Research Council scale and grade 5 in the remaining arm muscles. A Tinel’s sign was elicited in the supraclavicular fossa. Arm joints showed full range of motion. Neurophysiologic studies showed upper trunk plexopathy with denervation potentials present in the biceps brachii.

A new MRI scan was performed, which revealed a tumor in the left retroclavicular region, with complete involvement of the entire brachial plexus at the level of the trunks, divisions and fasciculi, and the subclavian artery, which was inside the tumor, and partial involvement of the subclavian vein. The tumor was in direct contact with the first rib and the lung apex, with no apparent infiltration of the ribcage. Definition of the top of the tumor was lost due to the area of postsurgical fibrosis with tumor infiltrate (Figs. 1A–C).The patient underwent surgery under general anesthesia, with a transsternal transclavicular approach. An incision was made through the scar from the previous biopsy and extended medially to the contralateral sternoclavicular joint and laterally to the deltopectoral groove. The subcutaneous tissue and platysma were cut and 2 large flaps were retracted to provide a broad exposure of the sternal manubrium, the clavicle and sternocleidomastoid muscle, and the entire supraclavicular fossa. The sternocleidomastoid muscle was defined before and after its insertion, as it needed to be spared, together with the periosteum covering the clavicle and the sternum. The pectoralis major muscle was disinserted from the medial lower half of the clavicle and from the upper part of the sternum to reveal the costosternal joint, and the sternoclavicular joint capsule wasspared. Osteotomy of the clavicle was performed after removing a small amount of periosteum from the middle third of the clavicle. An inferior dissection was performed at the incisura jugularis using delicate periosteotomes and blunt dissectors, and a malleable retractor was inserted. The space between the costosternal joints of the first and second ribs was identified and another malleable retractor was inserted until it met the other retractor. The purpose of the retractors was to provide protection while performing 2 delicate L-osteotomies using a fine osteotome or a sternotomy saw on the left upper outside angle of the manubrium, including the sternoclavicular

FIGURE 1. Preoperative MRI of case 1. AFIGURE 1. Preoperative MRI of case 1. A, Coronal image showing the tumor located in the supraclavicular and retroclavicular region, extending from the trunks to the fasciculi of the left brachial plexus. B, Coronal angio-MRI showing involvement of the subclavian vessels. C, Sagittal image showing how the tumor completely encompasses the subclavian artery and partially encompasses the subclavian vein.

Intraoperative photographs of case 1FIGURE 2. Intraoperative photographs of case 1. A, Retraction of the osteomuscular flap with the upper angle of the sternum,
the sternoclavicular joint and the medial half of the clavicle over the sternocleidomastoid muscle, and exposure of the tumor.
B, Intraoperative picture after total resection of the tumor. The image shows the complete liberation of the entire brachial
plexus and the subclavian artery and vein. The iatrogenic lesion of the anterior division of the upper trunk with no severe
functional repercussions can be seen. The osteomuscular flap can be seen in the upper left of the image. C, Intraoperative
photograph after repair of the anterior division of the upper trunk with six 2.5-cm long sural nerve grafts.

joint and the costosternal joint of the first rib, while sparing the entire insertion of the sternocleidomastoid muscle in the clavicle and in the sternum. The costosternal cartilage of the first rib attached to the sternum was cut using a scalpel. The medial half of the clavicle and the left upper outside angle of the sternum were elevated toward the cranium, joined by the sternoclavicular joint on the sternocleidomastoid muscle. The entire osteomuscular flap was wrapped in a damp pad. The sternohyoid muscle and subclavian muscle were exposed. Cutting these muscles made it possible to expose the entire tumor completely surrounding the brachial plexus, from the trunks to the fasciculi. The subclavian artery encompassed completely by the tumor and the subclavian vein partially. The vessels and nerves above and below the tumor were identified. The subclavian artery and vein were first completely freed; this operation required an intratumor access route. All the nerves of the plexus were dissected to reveal a postbiopsy iatrogenic section of the anterior division of the upper trunk, and the tumor was resected completely (Figs. 2A, B). Intraoperative electrostimulation was used in locating the damaged nerve. The lesion was repaired with 6 sural nerve grafts of 2.5-cm taken from the right leg; the grafts were sutured using fibrin glue (Fig. 2C). The sternum was closed using reabsorbable bone sutures and the osteosynthesis of the clavicle was performed using a minifragment titanium plate. The patient’s clinical course revealed that feeling was regained in the first 2 fingers, together with clavicular pseudarthrosis was observed, which required further surgery to perform an iliac-crest bone graft and repeat osteosynthesis;
the osteosynthesis was consolidated and the patient regained function of the limb with no differences compared with the contralateral limb. The 3-year follow-up revealed no symptoms or radiographic signs of tumor recurrence. Medical Research Council grading system graded 5 power in all arm muscles. All arm joints maintained full range of motion.

Microscopic and pathologic examination revealed neoplastic proliferation consisting of fusiform cells with a large cytoplasm, and a large nucleus with a clearly visible nucleolus. Many inflammatory cells were observed between these cells, together with focal presence of osteoclast-like giant cells. The lesion extended to the margin of the resection. Immune staining was positive for vimentin externally and focally positive for ALK-1 and actin. Necrosis foci were observed. Mitosis was rare. Twenty percent of the tumor cells stained positive with Ki-67. The histopathology diagnosis was an inflammatory myofibroblastic tumor (IMT).

Case 2

A 16-year-old boy visited his doctor because of a growth in the left subclavicular region. The patient experienced no pain or neurologic deficiency. He was referred to the thoracic surgery department where an MRI scan of the region was performed; the scan revealed a subclavicular tumor in close contact with the brachial plexus, and the patient was therefore referred to our unit.

FIGURE 3. Preoperative MRI of case 2. A, Axial image showing the tumor located in the retroclavicular and subclavicular region,
extending between the divisions and fasciculi of the left brachial plexus. B, Axial image in another MRI sequence showing
compression of the subclavian vessels and the brachial plexus. C, Coronal image showing how the tumor encompasses
the fasciculi of the brachial plexus.

FIGURE 4. Intraoperative photographs of case 2. A, Transsternal transclavicular approach that allowed for resection of the tumor. The photograph shows the broad exposure of the subclavian vessels from the mediastinum to the axilla and exposure of the entire brachial plexus. B, Photograph of the resected part marked with stitches. C, Intraoperative picture of the reconstruction of the approach, with cerclage wire in the sternum and a DCP in the clavicle.

Tests revealed a tumor measuring 10 x 7.5 cm, which appeared to originate in the pectoralis minor and extend to the retroclaviculararea, from the sternoclavicular joint to the axilla. The upper lateral end of the lesion met with the coracoid apophysis of the scapula and with the deltoid muscle. The tumor was compressing the subclavian vessels, but these were still patent. The brachial plexus was being pushed toward the posterior side, with no visible infiltration, although it was in close contact with the tumor (Figs. 3A–C). An ultrasound-guided percutaneous biopsy was performed in the region of the axilla and revealed low-grade mesenchymal infiltration suggestive of fibromatosis. The patient underwent surgery under general anesthesia, with a transmanubrial transclavicular approach identical to that of the first patient, with osteotomy of the upper quadrant of the sternum and osteotomy of the clavicle. The subclavian vessels and brachial plexus were identified after dissecting and separating the tumor, and no infiltration was observed (Fig. 4A). We performed a subtotal extirpation of the pectoralis major and total of the pectoralis minor; these muscles were infiltrated and the tumor was not exposed at any time. The tumor had also infiltrated the tip of the coracoid apophysis, which therefore required resection at its base (Fig. 4B). Reconstruction of the sternum was performed using cerclage wire and osteosynthesis of the clavicle was performed using a 6-hole dynamic compression plate (Fig. 4C). The results of the anatomic pathology study revealed musculoaponeurotic fibromatosis in contact with the surgical margin at 1 point. The oncology department decided to instate adjuvant radiation therapy in the postoperative period. The postoperative clinical course was satisfactory and the patient experienced no limitations of shoulder movement or neurologic deficiency in the limb. Radiologic examinations in the follow-up period revealed consolidation of the clavicle, which was determined by means of a computed tomography scan a year after the operation. Follow-up clinical and imaging examinations revealed no recurrence 2 years after the resection.

DISCUSSION

IMTs and desmoid tumors are true benign solid tumors; they are rare and affect children and young adults. Although these tumors are histopathologically benign, they cannot be differentiated from malignant tumors due to their local invasiveness and their tendency to recur.1 The location of the IMT in the peripheral nerves is exceptional,2–4 and we have found no reported cases in the brachial plexus. In some cases, IMT may become malignant.5–7 According to the literature, presentation of desmoid tumors in the brachial plexus is not so exceptional.8–9 The only treatment that has been shown to be effective in managing these tumors is total surgical resection in both primary and recurring tumors. In most cases, other measures such as chemotherapy and radiation therapy should be avoided, as they are ineffective and aggressive for a tumor with limited biologic potential.

However, there is a considerable incidence of postoperative recurrence, ranging from 8% to 37%.8–13 Tumor locations that make resection difficult, as in our cases in the brachial plexus, make treatment difficult. Resection of the tumor is associated with a considerable risk to the structures involved or encompassed by the tumor and alternative treatment, such as chemotherapy and radiation therapy, are ineffective on their own and are only used as adjuvant therapy.8 –9,11 Radiation therapy causes fibrosis and makes resection considerably more complicated, particularly in cases of recurrence.

The inability to resect a slow-growing tumor in a young person or child is a dramatic situation that causes anxiety in the patients and their family members. As occurred, in these cases, these are patients who have already experienced multiple visits to doctors and different surgical departments, where they were initially told that the tumor could not be resected.

The decision to operate was taken, although resection of lesions in this location requires experienced surgical teams.The supraclavicular approach frequently used to examine the trunks of the brachial plexus or decompressions in thoracic outlet syndrome does not allow for examination of the retroclavicular plexus. The standard transclavicular approach of Fiolle and Delmas (1921) is usually carried out to examine and repair the brachial plexus in cases of traumatic injury. This approach affords broad access to the entire brachial plexus, but only provides limited access to the more medial and mediastinal structures (lower trunk and divisions), and it does not provide complete exposure of the vascular structures, especially in the more medial part.

In tumors of the brachial plexus that involve the large vessels and the lower trunk and divisions, a more extensive approach such as the transmanubrial transclavicular approach is preferable. The description of this approach has been attributed to Sundaresan, but he resected the bone segment and therefore killed part of the sternal manubrium and the medial portion of the clavicle, which he used as grafts in tumors of the second to fourth dorsal vertebrae.14 However,
the first description of this approach based on the retraction of an osteomuscular flap that allows for reconstruction and spares the sternocostal joint was reported by Bonney in 1976.15 Although a large amount of bone is retracted, vascularization is maintained via the insertion of the sternocleidomastoid muscle. However, it was Birch who published the only series of 17 cases in different applications (spinal tumors, cervicothoracic scoliosis, soft-tissue tumors, T2-T3 disc hernias, osteomyelitis of the first rib, and neuritis of the brachial plexus) and publicized its use in tumors of the brachial plexus.16,17 This approach is technically highly demanding and requires experience in vascular surgery and neurosurgery, and considerableknowledge of the anatomy of the area; however, it does afford excellent exposure of all the structures and control of the proximal great vessels. The complications in the Birch series included pneumothorax in 30% of cases and pseudarthrosis of the clavicle in 23% of cases, although 3 patients died in the follow-up period. We observed pseudarthrosis in the younger patient, in whom we used a mini-fragment titanium plate that broke after a year.

Webelieve that this complication can be minimized by using modern preformed compression plates and locking screws, and by sparing the periosteum connected to the sternocleidomastoid muscle, as performed in the second case. No cases of sternal pseudarthrosis
were observed in the Birch series or in our patients.16,17

We believe that it is an appropriate approach for resecting tumors of the brachial plexus provides broader exposure and allows for decompression and direct viewing of the entire plexus and vascular structures. The approach also allows for suitable reconstruction, with only a moderate risk of clavicular pseudarthrosis.
Familiarity with the anatomy of the area and a careful dissection technique ensure adequate access with the minimum amount of complications.

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