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Epiphyseal fibula transfer to proximal humerus following resection for osteosarcoma

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The proximal humerus is the fourth most common site for primary bone sarcomas, with up to 15% of osteosarcomas and 10% of Ewing’s sarcomas occurring at this site. Preserving growth and function following limb-salvage surgery in paediatric patients remains a challenge, as the proximal humeral physeal growth is responsible for 80% of the total growth of the humerus, and loss of one of the physes is associated with limb-length discrepancy. This is particularly challenging in small children in whom endoprosthetic replacements are often too large and expandable prostheses have higher rates of complications compared with adults.
Vascularised autografts may provide rapid biological incorporation with the potential for growth and a limb-salvage reconstruction with longevity.
Vascularised fibular epiphyseal transfer preserves function and growth in young children following excision of the proximal humerus for a malignant bone tumour. Function compares favourably to other limb-salvage procedures in children. Failures are caused by avascular necrosis of the graft but the reported survival of the reconstruction is 82% at five years.
Author: Mr Jonathan Stevenson FRCS (Tr & Orth)
Institution: The Royal Orthopaedic Hospital ,Birmingham ,UK.

INDICATIONS
Reconstruction following wide resection of bone tumours of the proximal humerus in adults is reliably addressed with endoprostheses, which are associated with comparable function, fewer complications, and longer durability than allograft-prosthesis composite, osteoarticular allograft, or clavicular pro humero reconstructions. Preserving growth and function following limb-salvage surgery in paediatric patients remains a challenge, as the proximal humeral physeal growth is responsible for 80% of the total growth of the humerus, and loss of one of the physes is associated with limb-length discrepancy. This is particularly challenging in small children in whom endoprosthetic replacements are often too large and expandable prostheses have higher rates of complications compared with adults.
Cadaveric anatomical research during the 1980s identified reliable blood supply to the proximal epiphysis and the proximal two-thirds of the diaphysis of the fibula from the anterior tibial artery. Developed by Marco Innocenti of Florence, this became the preferred pedicle for vascularised transfer of the proximal fibular epiphysis to reconstruct the proximal humerus and distal radius, showing evidence of graft hypertrophy and longitudinal growth at the epiphysis. Vascularised epiphyseal transfers have the advantage of more predictable growth and prevent premature physeal closure when compared with non-vascularised grafts, and rapid autograft incorporation in limbs compromised by chemotherapy or radiotherapy. These rare and demanding operations require careful pre-operative discussion with parents and liaison with plastic surgery colleagues.
SYMPTOMS & EXAMINATION
Patients with primary bone tumours present principally with pain and swelling, with or without limitation of motion (and reduced ability to bear weight in the lower limb).
Biopsy tract, range of motion of the shoulder and elbow, deformity, neurovascular status, skin quality including previous scars and sinuses, deltoid function, regional lymphadenopathy and availability of local soft tissue flaps should all be considered in the clinical examination.
IMAGING
Plain radiographs usually delineate the size and location of the tumour as well as any extra-osseous extension. Radiographs are assessed for the extracellular matrix deposition of the tumour be that osteoid (e.g. osteosarcoma), chondroid (e.g. chondrosarcoma) or fibrous (fibrosarcoma of bone) which hints at the diagnosis. The age and anatomical location (epiphyseal, metaphyseal, diaphyseal) are important clues in narrowing the differential diagnosis.
In the proximal humerus necessary radiographs include measured radiographs of the whole humerus AP and lateral and including the gleno-humeral and elbow joints.
Patients undergo biopsy to confirm the histological diagnosis. In our centre biopsies either occur in the operating theatre using a Jamshidi needle and fluoroscopy or CT guidance typically via a deltopectoral approach. The positioning of the biopsy tract is crucial to ensure that is does not cross more than one anatomical compartment or compromise vital structures as the biopsy tract is excised en-bloc at the time of surgery. Typically the histological biopsy results take 7 to 10 days to be reported and are discussed at the sarcoma multi-disciplinary team (MDT) meeting comprising orthopaedic surgeons, radiologists, pathologists and oncologists.
Prior to surgery patients are ‘staged’, which involves local staging of the affected bone (i.e. MRI scan of the whole humerus including the gleno-humeral and elbow joints) and distal staging (CT chest and whole body bone scintigraphy) to exclude metastatic disease. If metastases are identified at the time of diagnostic staging this may influence the extent of surgical and systemic treatment but may not preclude surgical excision of the primary tumour; all of these details are considered at the sarcoma MDT when deciding upon the optimum treatment by all involved specialists.
ALTERNATIVE OPERATIVE TREATMENT
For primary malignant bone tumours of the proximal humerus, alternatives to vascularised fibula autograft reconstruction include endoprosthetic replacement, allograft or allograft prosthetic composite. Endoprosthetic replacements are the most commonly used limb-salvage reconstruction of the proximal humerus in our centre, however in very young children the residual bone is often too small to accept the stem of a prosthesis. Although ‘growing’ endoprostheses in this location have been used they may require multiple invasive lengthening procedures and the abduction and forward flexion are poor (https://online.boneandjoint.org.uk/doi/pdf/10.1302/0301-620X.81B3.0810495).
Allografts and allograft prosthetic composites reconstruct the proximal humerus with an allograft matched in all dimensions to the planned resection, secured with plates and screws. The latter involves pre-operative insertion of a prosthetic humeral component and then osteosynthesis of the allograft to the residual distal humerus. In some centres, allografts are augmented with vascularised fibula autografts (Capanna technique) to encourage host bone incorporation and minimise fracture and non-union rates.
NON-OPERATIVE MANAGEMENT
Osteosarcomas typically receive pre-operative chemotherapy, then surgical resection and limb-salvage followed by further post-operative chemotherapy. Some tumours, such as Ewing’s sarcoma are relatively sensitive to radiotherapy which may be a non-operative intervention in some appendicular Ewing’s sarcomas.
CONTRAINDICATIONS
If the patient was medically unfit to undergo major surgery or if the staging revealed that the disease had already spread to the lungs with a very poor prognosis then surgery may be contraindicated although palliative surgery to control pain may still be contemplated.

GA + spinal block, urinary catheter, arterial line
Supine with right upper limb and right lower limb isolated using drapes
Tourniquet right proximal thigh
IV Antibiotics (flucloxacillin and gentamicin), ultra clean theatre
Double alcoholic skin preparation, Ioban incisional drapes
Microscope prepared for vascular anastomosis

AP radiograph of the right humerus showing aggressive tumour at the proximal metaphysis with evidence of periosteal reaction and osteoid deposition.

T2 – weighted MRI coronal sequence showing soft tissue mass associated with proximal humeral osteosarcoma.

Fluoroscopic image showing Jamshidi core needle biopsy of proximal humeral osteosarcoma. The principles associated with biopsy of primary malignant bone tumours include ensuring that the trajectory of the biopsy does not cross multiple fascial compartments and can be cleanly excised at the time of surgical excision of the tumour.

AP radiograph of the whole humerus showing pathological fracture at the proximal metadiaphysis with angulation and ossification of the tumour after commencement of neoadjuvant chemotherapy.

T1 – weighted axial MRI sequence showing the 5x5cm osteosarcoma of the proximal humerus. This image is used to confirm the neurovascular bundle is clear of tumour involvement (seen medially) prior to en-bloc excision and limb salvage.

Patient positioning and limb isolation. Mark humeral skin incision. With the child anaesthetised the whole right upper limb is excluded using a U-drape with a sand bag under the right scapular to extend the glenohumeral joint.

Mark fibular skin incision. After placing a thigh high tourniquet above the right knee another U-drape has been used to exclude the entire right lower limb. The incision for harvesting the vascularised epiphyseal fibula graft is marked on the anterolateral aspect of the lower limb, proximally curved around the fibular neck. After skin cleansing with alcohol chlorhexidine the limb is draped and a glove placed over the foot.

Skin preparation and drape application.After alcohol chlorhexidine skin prep and draping the right humerus and shoulder are draped with IOBAN incisional drapes.

Skin incision. The initial excision of the tumour begins with an anterior approach along the humerus; landmarks for incision are from the coracoid process to the biceps tendon at the elbow.

Identify cephalic vein. The deltopectoral interval is identified by identifying and tracing the cephalic vein distally, to gain access to the proximal humerus. Blunt finger dissection is preferred to develop this plane between (D) deltoid and (PM) pectorals major with coagulation required of any branches to the cephalic vein from the deltoid muscle.

Release pectorals major.No.1 Vicryl stay sutures are placed into the (PM) Pectoralis major tendon for later reattachment leaving an adequate surgical margin on the tumour.

Viewed from the medial side now, the (M) musculocutaneous nerve is exposed and highlighted medial to the (B) biceps after exiting the (C) coracobrachialis. Also shown for orientation is the anterior head of the (D) deltoid muscle.

Tenodesis of long head of biceps.The (LHB) long head of biceps tendon is identified for tenodesis at the level of the metaphysis. The anterior bundle of the (D) deltoid muscle is clearly visualised in this photograph.

A No. 1 Vicryl stay suture is placed in the long head of biceps prior to tenodesis for later reconstruction.

After tenodesis of the LHB the rotator cuff interval is dissected using McIndoe’s dissecting scissors to gain access to the articular surface of the joint. The silver white capsule and subscapularis tendon are seen in the photograph.

Subscapularis stay sutures.The (ST) subscapularis tendon has stay sutures (No.1 Vicryl) inserted into its tendon before division.

Divide subscapularis tendon.The tendon of subscapularis is incised with cautery, using the stay suture for tension as shown.

After division of the subscapularis tendon, the (A) articular surface of the proximal humerus becomes visible. This will allow external rotation of the humerus, granting access to the joint and rotator cuff.

The dissecting scissors are now placed underneath the insertion of the (SSp) supraspinatus and infraspinatus tendons as they insert on to the greater tuberosity of the proximal humerus, prior to sequential release.

Divide the supraspinatus and infraspinatus tendons off the greater tuberosity.The (SSp) supraspinatus and infraspinatus tendons are released off the greater tuberosity using cautery.

Stay sutures into supraspinatus and infraspinatus tendons.After release of the insertion of the supraspinatus and infraspinatus rotator cuff tendons stay sutures are placed in to the (SSp) cut tendons for later reconstruction. The articular surface of the humeral head is clearly visualised.

Stay suture in teres minor. After placing a stay suture in to the (TM) teres minor tendon this is now released from the posterior aspect of the greater tuberosity using the stay suture to maintain tension as shown.

Release residual gleno-humeral joint capsule. Having released the rotator cuff tendons off the proximal humerus, dissection now continues posteriorly and inferiorly to release the capsular insertion on the humeral side of the joint working clockwise around the humeral metaphysis..

Identify and protect the auxiliary nerve.Dissection now progresses around the tumour keeping a cuff of normal tissue attached to the tumour for a surgical margin. Using the McIndoe’s dissecting scissors, the plane above the axilliary nerve as it courses posterior around the proximal humerus is dissected to protect the nerve as any residual capsular fibres are released.

After further dissection of the proximal humerus the deformity caused by the pathological fracture is evident and the tumour mass with soft tissue coverage can clearly be seen inferior to the humeral articular surface. The dissection has now progressed beyond the tumour to the humeral diaphysis.

Identify and preserve the radial nerve.Care is taken to preserve the radial nerve at the triangular interval using McIndoe scissors and careful use of the diathermy. The cut edge of Trees major is seen forming the superior border of the interval.

Dissect the proximal humerus leaving adequate soft tissue margin on the osteosarcoma.After further dissection of the proximal humerus the deformity caused by the pathological fracture is evident and the tumour mass with the soft tissue coverage can clearly be seen inferior to the humeral articular surface. The dissection has now progressed beyond the tumour to the humeral diaphysis.

Measure resection point.The resection level which was calculated pre-operatively using the T1 weighted MRI scan is measured using a metal ruler and a Kocher’s forceps.

The resection level is marked using diathermy on the humeral shaft. Distal to the resection level the bone is held with Heygrove’s bone holding forceps.

Humeral osteotomy using reciprocating saw blade. Using a 1.27mm reciprocating bone saw blade the humeral diaphysis is cut at the marked resection level. This photo shows the degree of soft tissue extension caused by the tumour.

The residual proximal humerus is shown after the resection of the humeral diaphysis resection level with the Heygrove’s bone holding forceps still holding the distal section.

Distal resection margin sampling.A medullary bone sample distal to the resection is obtained using a small bone curette and sent separately for axiological analysis routinely.

Photograph of the resected proximal humerus with soft tissue margin evident at the metaphysis overlying the osteosarcoma. Simultaneous to the resection of the proximal humerus the dissection and excision of the vascularised proximal fibula graft commences.

Fibular skin incision.Simultaneoulsy the vascularised proximal fibula graft is harvested by the plastic surgery team. The skin incision over the anterolateral aspect of the lower leg is marked.

Fibular inter-muscular dissection.The skin is incised anterolaterally and after dissection of the subcutaneous tissues, the fascia is incised leaving a cuff of fascia on the tibia to enable reattachment. Inter-muscular dissection is developed between (TA) Tibialis anterior and (EDL) Extensor digitorum longs proximally and Tibialis anterior and (EHL) Extensor hallucis longus distally.

Expose tibialis anterior vessels.The fascia is carefully incised up towards the proximal tibiofibular joint to expose the tibialis anterior neurovascular bundle. The common peroneal nerve is then identified proximally at the level of the fibular neck and protected.

Sloop the peroneal nerve.Sloops are placed on the peroneal nerve distally and proximally.

The origin of the peroneii and extensor digitorum longus are released 2cm from the proximal fibula to enable visualisation of the peroneal nerve and its branches as it courses around the fibula neck, the (P) peroneal nerve can then be traced distally between the bellies of the peroneal muscles. The (MC) muscular cuff left intact around the fibular epiphysis reduces the risk of damaging the recurrent epiphyseal branch or the anterior tibial artery which supplies the growth plate and epiphysis.

A hand held doppler probe is used to confirm the position of the anterior tibial artery as it courses through the inter-osseous membrane into the anterior compartment of the leg.

Measure and osteotomise the distal fibular resection point.After measuring the length of resected proximal fibula which is required for the vascularised graft which is determined by the length of humerus resected and oscillating hand held saw is used to bisect the fibula shaft distally.

The periosteum is preserved as the fibula is dissected from distal to proximal here being held by bone holding forceps distally to elevate it off the interosseous membrane.

This photograph shows the branches of the peroneal nerve as they course around the fibula neck with branches going to the peroneal muscles and to the extensor digitorum and tibialis anterior muscles.

A liger clip is used to ligate the collateral medial branches of the anterior tibial artery with the dissected peroneal nerve elevated for protection.

Harvest the vascularised fibular graft and ‘Z’ plasty of the biceps femurs tendon.The vascularised fibula graft being harvested from the leg.
The tendon of biceps femoris is longitudinally divided off the fibular head (‘Z’ plasty), of which a posterior strip is harvested with the fibula graft to be used to stabilise the epiphysis in the arm. The anterior strip is used to reinforce the lateral collateral ligament during closure of the lower limb wound.

This shows the resected vascularised proximal fibula graft placed on the back table prior to implantation in the proximal humerus.

The fibula bed is shown after tourniquet deflation to achieve haemostasis. The (P) peroneal nerve and it’s preserved muscular branches to (TA) tibialis anterior are shown.

Bone anchor into proximal tibial metaphysis to reconstruct lateral collateral ligament and biceps femoris tendon. A bone anchor is placed in to the proximal tibial metaphysis with care used to avoid the physeal growth plate. This bone anchor has sutures attached which is to be used for re-attachment of the anterior strip of the of the biceps femoris tendon and the lateral collateral ligament both of which are released off to the proximal fibula epiphysis.

Irrigation of the wound prior to closure in layers.

Layered fibula wound closure.The wound is closed in layers with a suction drain exiting distally.

Subcutaneous 3.o PDS sutures are used to close the skin.

The microscope used by the plastic surgical team to prepare the brachial vessels to dissect out the brachial vessels for anastomosis to the vascularised fibula graft.

Microsurgical instruments are used to dissect axilliary vessels free for the vascular anastomosis.

Microsurgical vascular anastomosis of the fibular graft.A vein graft has been used to lengthen the vein graft to ensure that there is adequate length for the anastomosis to take place without undue tension.

The fibula graft is placed in to the proximal humeral bed to check for the appropriate length and rotation with the articular surface of the proximal fibula facing the glenoid. The muscle cuff proximally containing the delicate recurrent epiphyseal branches of the anterior tibial artery is seen covering the non-articular fibula head.

Osteosynthesis of the fibula graft to the residual distal humerus. A 5-hole 1/3 tubular plate is selected and used to osteosynthesise the proximal fibula to the residual distal humerus. Plate holding forceps are used to adjust and temporarily hold the plate in position.

Small fragment 3.5mm cortical screws are used to compress the osteotomy site.

After osteosynthesis the fibula can be seen to have been attached to the residual distal humerus.

A bone anchor is placed in to the centre of the glenoid articular surface for attachment to the residual posterior slip of biceps femoris tendon on the proximal fibula epiphysis to improve stability of the vascularised fibula graft.

The fibula graft has been placed in to the humeral bed, the stay sutures for the rotator cuff tendons are evident and the (PF) proximal fibula articular surface is effacing the glenoid.

Graft jacket sling for fibula head.A 5cm strip of graft jacket matrix scaffold (Wright Medical) is sutured to the posterior and anterior aspects of the glenoid to form a sling to retain the proximal fibula epiphysis for stability. This is sutured using No 1 Vicryl tied sutures.

After preparation of the graft jacket the sling around the proximal fibula is evident. The stay sutures of the rotator cuff are attached to the graft jacket, to help form and stabilise neo-glenohumeral joint for the fibula graft.

Soft tissue reconstruction of anterior shoulder muscles.The long head of biceps is tenodesed to the anterior glenoid where the graft jacket is inserting. Fibres of the (D) deltoid, (C) coracobrachialis, (B) biceps and (PM) pectoralis major tendon with stay suture are evident. The pectorals major tendon is sutured to the anterior fibres of deltoid as the final muscular reconstruction.

Layered wound closure. The wound is closed in layers with interrupted No.2.0 Vicryl sutures to the subcutaneous tissues.

Skin closure. The skin is closed with subcuticular 3.0 PDS sutures.

Apply dressings.The wound is dressed with an aquacel dressing and a sling is applied.

The lower limb is wrapped in wool and crepe and placed in to a splint for pain relief and wound healing.

Immediate post-operative radiograph of the right proximal humerus with the vascularised fibula graft and multiple surgical clips evident or in the anastomosis. The 1/3 tubular plate used for epiphysis on the osteotomy is evident and the component placed in to the glenoid is also shown.

Three months following reconstruction a rotated anterior view is showing evidence of Harris growth arrest lines indicating that the growth at the proximal fibula bioseal plate has been maintained.

Post-op radiograph of the right lower limb showing multiple vascular clips following resection of the proximal fibula and the bone anchor placed in to the metaphysis of the proximal tibia for re-attachment of the biceps femoris and lateral collateral tendon and ligaments respectively.

High dependency level care.
Neurovascular observations of both the right upper and lower limbs.
Antibiotics for 24 hours.
Sling to be maintained without passive movement for six weeks and then passive movement of the neo-glenohumeral joint under physiotherapy guidance from weeks six to eight.
Check radiographs and commencing active motion, further X-rays at three months of the whole humerus.
A hinged knee brace to be applied to the knee to prevent coronal instability for eight weeks.
Wheelchair until brace removed from the knee.
MDT discussion of histology results: Histology has confirmed 95% necrosis and wide margins of growth in 2mm of the neurovascular bundle medially.

There is a paucity of data describing the outcome of this procedure in children for primary bone sarcomas. At a mean follow-up of 5.2 years, Stevenson et al. reported a rate of limb-salvage of 100% and a rate of overall survival, local recurrence and metastasis of 91% (https://online.boneandjoint.org.uk/doi/full/10.1302/0301-620X.100B4.BJJ-2017-0830.R1).
Manfrini M , et al. Evolution of surgical treatment for sarcomas of proximal humerus in children: retrospective review at a single institute over 30 years. J Pediatr Orthop 2011;31:56–64.
The mean functional MSTS score of 77% reported by Stevenson is identical to that reported by Manfrini et al. in eleven children with the same reconstruction, and slightly inferior to the 80% in their three allograft-prosthetic composite patients
Emori M, et al . Vascularised fibular grafts for reconstruction of extremity bone defects after resection of bone and soft-tissue tumours: a single institutional study of 49 patients. Bone Joint J 2017;99-B:1237–1243.
The mean growth at the transplanted proximal fibular epiphysis was 4.6 mm per annum in the grafts that did not develop avascular necrosis. 18% did develop avascular necrosis of the graft, which was in keeping with previous studies by Manfrini et al. and Emori et al.


Reference

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