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Ann Thorac Surg 1996;61:525-529
© 1996 The Society of Thoracic Surgeons


Original Article: General Thoracic

Bone Heterograft for Chest Wall Reconstruction After Sternal Resection

Francesco Puma, MD, Nicola Avenia, MD, Francesco Ricci, MD, Antonio Guiducci, MD, Vittorio Fornasari, MD, Giuliano Daddi, MD

General Thoracic Surgery Unit, Department of Surgery (R), University of Perugia Medical School, Terni, Italy

Accepted for publication October 2, 1995.


    Abstract
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 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 
Background. Experimental and clinical results of chest-wall reconstruction with bone heterograft after sternectomy are reported.

Methods. Seven dogs underwent subtotal or total sternectomy and reconstruction by implantation of a cortico-spongy bone heterograft sandwiched between two layers of a reabsorbable mesh.

Results. No major postoperative complications were observed. The implant has shown favorable mechanical and biological properties. Six and 9 months after operation all animals were sacrificed and pathologic examination showed good incorporation of the implanted bone with only partial resorption of its spongiosa. Subsequently, 2 patients underwent sternal resection with different indications and reconstruction was achieved by the technique developed experimentally. No complications were observed. Excellent immediate chest-wall stabilization was obtained, persisting for a follow-up period longer than 6 months.

Conclusions. In comparison with autologous bone, sterile bone heterograft seems to offer the same mechanical properties with a significantly reduced surgical trauma.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 
Chest wall stabilization after total sternectomy is a technical challenge for the thoracic surgeon. Sternal resection is generally required for treatment of both primary and secondary neoplasms and osteomyelitis due to wound infection after median sternotomy.

The great majority of sternal tumors are malignant, chondrosarcoma being the most frequent [1]. Benign tumors are rare, although malignant degeneration is possible [2].

Wide resection represents the key to successful treatment of sternal tumors. Total sternectomy is generally advised because the disease may spread through the bone marrow. Removal of the entire sternum might require complex reconstructive procedures depending on the preexisting anatomofunctional situation. Protection of intrathoracic organs and restoration of physiologic ventilatory dynamics generally warrant the use of rigid materials (autogenous or prosthetic). Different surgical techniques have been described for sternal reconstruction, although at present the ideal procedure seems far from being attained.

This article reports technical details and experimental and clinical results of chest wall stabilization after sternectomy using heterologous bone graft.


    Experimental Research
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 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 
Material and Methods
Seven female beagles aged 12 to 24 months are included in the study. All animals received humane care in compliance with the ``Guide for the Care and Use of Laboratory Animals'' published by the National Institutes of Health (NIH publication 85-23, revised 1985).

The dogs were submitted to operation under general anesthesia with endotracheal intubation. Anesthesia was induced with sodium thiopental 2.5% (6 mg/kg intravenously) and maintained with oxygen, nitrous oxide, and halothane (1.5% to 2.0%).

In the first group (5 dogs) subtotal sternectomy was carried out. The animals were placed in supine position and the skin was prepped with a solution of povidone-iodine. Skin and pectoralis major fascia were incised on the midline; sternal plate and costal cartilages were prepared and sternal resection was carried out with a Gigli saw, preserving only the first and the last sternebra. Both pleural cavities were entered, and ventilation was maintained mechanically. For the reparative phase a cortico-spongy bone heterograft was employed (Surgibone; Unilab, Hillside, NJ). This is a sterile bone implant of bovine origin chemically defatted and deproteinized, which proved to have no cytotoxic and pyrogenic effects and does not elicit immunologic or inflammatory reactions [3]. To facilitate implantation and incorporation of the prosthesis the bone heterograft was sandwiched between two layers of polyglactin reabsorbable mesh (Vicryl mesh; Ethicon, Somerville, NJ). The prosthesis was implanted with the mesh anchored to the ribs and to the sternal stumps with 2/0 Vicryl interrupted stitches. No chest drain was left in place. The pectoralis major fascia and the cutaneus trunci muscle were sutured over the prosthesis.

In a second group of 2 animals chest-wall repair after total sternectomy was carried out. Two bone heterografts were used in each dog (Fig 1Go a, b), arranged to maintain the physiologic contour of the canine sternum. The bone graft was sandwiched between two layers of Vicryl mesh (Fig 1Go c, d) and anchored to the rib stumps with transfixed nonabsorbable stitches while the mesh was sutured to the intercostal muscles (Fig 2Go).



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Fig 1. . Experimental technique: total sternectomy. (a, b) Two bone grafts are articulated so that the physiologic contour of the sternum is preserved. (c) Multiple holes are drilled in the bone graft, which is wrapped in Vicryl mesh. (d) The bone grafts are secured within the mesh.

 


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Fig 2. . The bone graft is anchored to the rib stumps with transfixed nonabsorbable stitches. The mesh is sutured to the intercostal muscles.

 
A prophylactic antibiotic regimen was started immediately postoperatively and maintained for 6 days. Postoperative chest x-ray films were taken at days 1 and 30.

Considering the dog's life span and its high metabolic rate, a maximum of 9 months of follow-up was deemed sufficient for long-term evaluation. All animals were sacrificed between 6 and 9 months by intravenous administration of barbiturates and curariform drugs. Pathologic examination of the chest wall was then performed.

Results
Postoperative course was uneventful in all animals but 1 in the second group in which wound infection developed, which resolved after dressings and antibiotic therapy without rejection of the implanted prosthesis. All animals resumed the physiologic prone position from the first postoperative day. Excellent short-term and long-term stabilization was achieved, and cosmetic results were considered satisfactory in all cases. Normal activity was resumed by all animals within 10 days after the operation.

Postoperative chest roentgenograms showed correct position of the prostheses in all animals but 1, in which a slight caudad displacement was detected. Such a complication had no clinical implications. Radiologic examinations did not reveal any resorption of the heterologous bone graft.

There were neither occurrence of late infection nor problems related to the biological tolerance of the prostheses.

Pathologic study showed complete reabsorption of the Vicryl meshes; heterologous bone graft was firmly attached to the sternal and rib stumps and incorporated into the mediastinal tissues on the spongiosa side, which was only partially reabsorbed. Neither incorporation nor resorption of the cortical plate was found. The specimen was placed in decalcifying solution for 24 hours. Microscopic examination revealed bundles of fibrous connective tissue surrounding bone tissue and bone trabeculae. Small buds of vascular connective tissue with a mechanism of osteoconduction ingrow into the Haversian canals of the grafted bone (Fig 3Go) and several multinucleated osteoclast-like cells responsible for peripheral spongiosa resorption were observed, particularly in the 9-month-old specimens (Fig 4Go).



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Fig 3. . Six-month-old specimen showing small buds of vascular connective tissue with a mechanism of osteoconduction ingrow into the Haversian canals of the grafted bone. (Hematoxylin and eosin; x250 before 55% reduction.)

 


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Fig 4. . Nine-month-old specimen showing several multinucleated osteoclast-like cells responsible for peripheral bone resorption. (Hematoxylin and eosin; x400 before 55% reduction.)

 

    Clinical Experience
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 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 
Patient 1
Patient 1 was a 56-year-old woman who, 6 years previously, had been submitted elsewhere to left radical mastectomy for breast carcinoma (pT2 N1 M0) followed by chemotherapy. No evidence of disease was demonstrated until January 1995, when the patient was referred to us for a substernal recurrence with bone invasion. The clinical work-up was carried out with computed tomographic scan and whole-body bone scan (focal area of increased uptake in the sternal body).

The operation was conducted through a median sternal incision. The operative finding showed bilateral extranodal metastases to the internal mammary chains, invading the sternum at the level of the third intercostal space. The upper three quarters of the sternal body was resected and stabilization achieved by inserting a molded bone heterograft into the medulla of the residual sternal stumps. As in the experimental technique the bone graft was sandwiched between two Vicryl meshes and the latter were sutured to the intercostal muscles. The pectoralis fascia was reconstructed over the prosthesis. Two pleural drains and one mediastinal drain were inserted. A prophylactic antibiotic regimen was started immediately postoperatively. The postoperative course was uneventful, and excellent immediate and long-term chest wall stabilization observed. Roughly 1 month after operation the patient was submitted to chemotherapy. Six months later magnetic resonance imaging showed the correct position of the prosthesis without local recurrence or reabsorption of the grafted bone.

Patient 2
A 39-year-old man was referred for solitary sternal myeloma, which presented itself a few months earlier as a painless mass on the anterior chest wall. The clinical work-up was conducted elsewhere with sternal biopsy, computed tomography, and magnetic resonance imaging of the thorax (Fig 5Go), whole-body bone scan, and roentgenography of the entire skeleton. A median sternal skin incision was carried down to the pectoralis fascia, which was left adherent to the tumor wall. Operative findings showed an apparently intact manubrium with complete involvement of the sternal body by friable soft tissue. Subtotal sternectomy was performed, preserving only the upper half of the manubrium; all the costal cartilages but the first were included in the resected specimen. Reconstruction was achieved by inserting a bone heterograft into the medulla of the residual manubrium and anchored with transfixed nonabsorbable sutures. The bone graft was sandwiched between two layers of polypropylene mesh (Prolene mesh, Ethicon) and secured to the latter with interrupted, nonabsorbable suture. The mesh was then anchored to the intercostal muscles (Fig 6Go). One anterior mediastinal and two pleural tubes were placed bilaterally. A bipectoral advancement flap was completed before skin closure. As in patient 1 a prophylactic antibiotic therapy was administered for 6 days. After an uneventful postoperative course the patient was sent to the referring Oncology Department for chemotherapy. Ideal short-term and long-term stabilization was achieved with excellent cosmetic results. Magnetic resonance imaging performed roughly 5 months after operation showed the correct position of the prosthesis without local recurrence or resorption of the grafted bone (Fig 7Go).



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Fig 5. . (Patient 2.) Magnetic resonance image of the thorax showing neoplastic involvement of the sternal body.

 


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Fig 6. . (Patient 2.) Reconstruction after subtotal sternectomy by inserting a bone graft wrapped with Prolene mesh into the medulla of the residual upper half of manubrium.

 


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Fig 7. . (Patient 2.) Magnetic resonance image of the thorax (roughly 5 months after operation) showing correct position of the implanted prosthesis in the residual manubrium stump.

 

    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 
The ideal chest wall reconstruction technique after sternectomy should not entail heavy surgical trauma and should be fast, simple, and capable of providing adequate mechanical support to the rib cage. The materials used should be well tolerated and rigid enough to offer protection to the mediastinal organs as well as stabilization of the chest wall.

Muscular flaps seem to be suitable for reconstruction after sternal osteomyelitis because of the mediastinal stiffness and because rigid materials tend to become infected in such a contaminated field. In different circumstances the use of isolated muscle flaps does not ensure reliable stability of the chest wall after total sternectomy, and a rigid support is considered mandatory to ensure protection and stability of the mediastinum and to avoid prolonged intubation.

Theoretically autogenous bone tissue is preferable because it allows immediate restoration of a rigid surface without any problem of biological tolerance, achieving a sort of restitutio ad integrum. Usually autologous bone graft is harvested from the rib cage or from the iliac crest and further materials (autogenous or prosthetic) are required for the stabilization to be satisfactory [4, 5]. Several disadvantages limit the use of such osteoplasty: extensive surgical trauma, possible inadequacy of autologous material, and heavier ventilatory functional damage if a rib graft is used.

The prosthetic materials are generally preferred because they provide better stability with shorter and simpler surgical procedures. Several substances have been used including Marlex mesh [6, 7], methyl-methacrylate [8, 9], metal strips [10] and even Dacron fabric-enveloped hydroxyapatite [11]. However, the use of these materials is not totally devoid of complications, the most important being infection caused by inadequate incorporation or implantation in a contaminated field [12]. Methyl-methacrylate particularly has several disadvantages: it is poorly incorporated, rigid, and difficult to fix, and it needs to be fashioned extracorporeally owing to the risk of general toxicity if the resin is polymerized in situ [13]. Furthermore, it may be necessary to add steel mesh to prevent the possible fragmentation of the plaque [14]. For these reasons at the moment prosthetic materials should not be considered the ideal procedure for sternal reconstruction. However, the most frequently used prosthetic technique is still based on a methyl-methacrylate plate sandwiched between two layers of polypropylene mesh. Such a prosthesis might be rejected if contaminated and furthermore is never completely incorporated. Synthetic reabsorbable materials are suitable for chest-wall repair, as we previously reported [15], but in reconstruction after sternectomy they do not ensure a rigid surface to protect the mediastinum.

The use of bone heterograft enveloped in a Vicryl mesh allows complete incorporation as the Vicryl mesh is totally absorbed and partial resorption is documented for the spongy compound of the bone heterograft, so that late infections are theoretically less likely to occur. In our second clinical case we decided to wrap the bone graft with a synthetic nonabsorbable mesh because of the wide resection in a heavy patient with a probable long life expectation. In this circumstance Prolene mesh might be preferable because it ensures both the complete incorporation of the bone graft and its definitive position.

The advantages of heterologous bone grafts in sternal reconstruction are the following: (1) The material is readily available and surgical trauma is reduced compared with the use of autologous bone graft. (2) The surgeon can choose between various shapes and sizes of bone graft for correction of different defects. (3) Surgical techniques are faster and easier than with autologous tissue. (4) Bone heterografts are not vectors for transmission of human disease. (5) The prosthesis shows good biocompatibility without cytotoxic and systemic effects. (6) The spongy compound of the graft is easily vascularized and the cortical graft has no tendency to be reabsorbed. (7) Stability and protection of the mediastinum are excellent and mechanical properties of the prosthesis are suitable for implantation in areas subjected to significant stress.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 
Address reprint requests to Dr Daddi, Clinica Chirurgica Generale e Toracica, Ospedale Civile, Terni 05100, Italy.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Experimental Research
 Clinical Experience
 Comment
 References
 

  1. McAfee MK, Pairolero PC, Bergstralh EJ, et al. Chondrosarcoma of the chest-wall: factors affecting survival. Ann Thorac Surg 1985;40:535–41.[Abstract]
  2. Martini N, Huvos AG, Smith J, Beattie EJ. Primary malignant tumors of the sternum. Surg Gynecol Obstet 1974;138:391–5.[Medline]
  3. Nielsen IM, Ellegaard B, Karring T. Kielbone in new attachment attempts in humans. J Periodontol 1981;52:723–8.[Medline]
  4. Sherman JE, Salzberg A, Raskin NM, Beattie EJ. Chest wall stabilization using plate fixation. Ann Thorac Surg 1988;46:467–9.
  5. Beggs JH, McCoy DM. Reconstruction of the sternum and anterior chest wall using autologous tissues. South Med J 1991;84:655–6.[Medline]
  6. Eng J, Sabanathan S, Pradhan GN. Primary sternal tumors. Scand J Thorac Cardiovasc Surg 1989;23:289–92.[Medline]
  7. Ala-Kulju K, Luosto R, Ketonen P, Salo J, Heikkinen L. Primary tumours of the sternum. Scand J Thorac Cardiovasc Surg 1989;23:169–72.[Medline]
  8. Paris F, Blasco E, Tarazona V, Pastor J, Zarza AG, Padilla J. Total sternectomy for malignant disease. J Thorac Cardiovasc Surg 1980;80:459–62.[Abstract]
  9. Gabbay S, Bennett RD, Amato J, Cherny EJ. Controversies in management of sternal tumors. Ann Thorac Surg 1989;48:428–31.[Abstract]
  10. Borrelly J, Grosdidier G, Maestracci C. Exerese elargie d'une tumeur metastatique pulsatile du manubrium sternal. Reconstruction par attelles-agrafes a glissiere. Ann Chir 1987;41:498–501.[Medline]
  11. Shinjo K. Dacron fabric-enveloped hydroxyapatite prosthesis for sternal tumor defect: an autopsy report. Plast Reconstr Surg 1990;86:973–8.[Medline]
  12. Pairolero PC, Arnold PG. Thoracic wall defects: surgical management of 205 consecutive patients. Mayo Clin Proc 1986;61:557–63.[Medline]
  13. Eschapasse H, Gaillard J, Henry F, Fournial G, Berthoumieu F, Desrez X. Repair of large chest wall defects: experience with 23 patients. Ann Thorac Surg 1981;32:329–36.[Abstract]
  14. McCormack P, Bains MS, Beattie EJ, Martini N. New trends in skeletal reconstruction after resection of chest wall tumors. Ann Thorac Surg 1981;31:45–52.[Abstract]
  15. Puma F, Ragusa M, Daddi G. Chest wall stabilization with synthetic reabsorbable material. Ann Thorac Surg 1992;53:408–11.[Abstract]



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