Eur J Cardiothorac Surg 2008;34:870-874. doi:10.1016/j.ejcts.2008.06.038
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
Chest wall reconstruction with two types of biodegradable polymer prostheses in dogs
Xiong Qin,
Hua Tang,
Zhifei Xu*,
Xuewei Zhao,
Yaochang Sun,
Zhiyun Gong,
Liang Duan
Department of Thoracic Surgery, Chang Zheng Hospital, 2nd Military Medical University, Shanghai, China
Received 28 January 2008;
received in revised form 24 May 2008;
accepted 9 June 2008.
* Corresponding author. Tel.: +86 216 3610109x73351; fax: +86 216 3519824. (Email: xu_zhi_fei{at}yahoo.com.cn).
 |
Abstract
|
|---|
Objective: Currently, the choice of chest wall prosthesis remains a challenging problem for thoracic and reconstructive surgeons. The purpose of this study is to investigate the feasibility of newly developed biodegradable prostheses. Methods: Two types of chest wall prostheses made from degradable polymer, collagen coated polydioxanone (CCP) mesh and chitin fiber reinforced polycaprolactone (CFRP) strut, were developed and studied. Adult mongrel dogs were subjected to extensive resection and reconstruction of anterior-lateral chest wall, CCP mesh was used in six dogs, the combination of CCP mesh and CFRP strut was used in four dogs, and polypropylene (PP) mesh in two dogs, as contrast. Results: With good integration with tissue, CCP meshes maintained strength in the chest wall for more than 8 weeks and were completely resorbed within 24 weeks, and satisfactory short-term and long-term chest wall stabilization was achieved. The combined use of CCP mesh with CFRP strut provided a firmer chest wall in the early postoperative course. A mild wound infection developed in one animal with CCP mesh but resolved without sequelae, and no added complications were observed with the additional use of CFRP strut. Conclusions: Our experimental study shows that the CCP mesh and CFRP prosthesis were favorable for chest wall repair. The advantages of biodegradable copolymer give them promise as an excellent addition to the available reconstructive techniques currently in use.
Key Words: Biocompatible materials • Thoracic wall • Reconstructive surgical procedures
|
1. Introduction
|
|---|
Reconstruction of chest wall defects remains a very challenging issue for the reconstructive surgeon. Extensive chest wall defects, which result primarily from tumor (primary, recurrent, metastatic, or locally invasive), radiation necrosis, infection, or trauma, often require prosthetic repair to prevent flail chest and paradoxical breathing [1–3].
Over the years, many different types of materials have been introduced and used to replace the chest wall. Synthetic prostheses have gained increasing popularity as they provide better stability with shorter and easier surgical procedures. However, late wound complications such as prosthesis dislocation, infection, fistulas or dense scar tissue formation occur frequently in the chest wall reconstruction, related to the properties of the employed undegradable material [3,4]. In such circumstances, the prostheses have to be removed with another operation. In recent years the use of biogradable compounds in chest wall repair with favorable results has been occasionally reported which might avoid late complications while assuring satisfactory stability of chest wall in the early postoperative course [1,5,6].
We have collaborated with Shanghai Jiaotong University to design and prepare prosthetic degradable biomaterials used for repairing chest wall defects from 2005; two types of newly developed biodegradable synthetic polymer have been examined in a canine model as an alternative for chest wall reconstruction and compared with polypropylene (PP) mesh.
|
2. Material and methods
|
|---|
2.1 Chest wall prostheses
2.1.1 Collagen coated polydioxanone (CCP) mesh
A 3D rectangular braid was developed by forming collagen coating on the surface of a polydioxanone knitted mesh. The mesh (thickness: 1 mm; mesh pore size: 300 µm) was knitted with polydioxanone monofilament fiber by means of a special microcaliber knitting machine. To keep the mesh airtight, the knitted mesh was coated with a bovine collagen acidic solution (type I, 2.0 wt.%). After drying, the visceral side of mesh was then coated with chitosan solution (2.0 wt.%) to smooth the inner side and decrease adhesions.
2.1.2 Chitin fiber reinforced polycaprolactone (CFRP) strut
A composite of polycaprolactone (PCL)/chitin was prepared by means of melt mixing (Institute of Composite Materials, Shanghai Jiaotong University, Shanghai). Briefly, the composite was melt-extruded to thin plates (h''2 mm) and was then cut to strut (100 mm x 10 mm). Chitin fiber was added to PCL, which is a flexible biodegradable polymer, to reinforce the mechanical strength and modify its degradable process. More information about CFRP was described by Yang and Wu [7].
All prostheses were sterilized by ethylene oxide gas before implantation.
2.2 Animal experiments
Twelve adult mongrel dogs aged 2–4 years, weighing 15.9–20.6 kg, were used in this study. The same operative procedures were adopted in different groups. 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 pentobarbital (30 mg/kg intravenously) and maintained with ketamine hydrochloride (2 mg/kg intravenously) and atracurium besylate (0.3 mg/kg intravenously) throughout the procedure. Ventilation was maintained mechanically after intubation. The dogs were placed in the lateral position and the skin was shaved and prepared with a solution of povidone iodine. An incision was made vertically to the rib in the right anterolateral region. The latissimus dorsi and the serratus anterior muscles were divided. In each dog, 8 cm segments of the consecutive three ribs [6–8] were resected in the midportion, including the intercostal muscles and the underlying parietal pleura. After completion of the resection, the skeletal chest wall defect was closed by use of three types of prosthesis. CCP mesh was employed in six dogs; CCP mesh, in conjunction with CFRP strut, was used in four dogs; and the other two, as contrast, with PP mesh. CCP mesh and PP mesh, measuring 8 cm x 8 cm, were sutured under tension to the superior and inferior rib with a large needle and surrounding interposed soft tissue with nonabsorbable interrupted sutures. In the combinational group, CFRP strut was first firmly anchored inside the CCP mesh to two sections of resected rib with steel wire (Fig. 1
). A pleural drain was inserted and the muscular layers were sutured over the prosthesis. Subcutaneous tissue and skin were closed layer by layer, with a subcutaneous negative pressure drain left in place.
View larger version (151K):
[in this window]
[in a new window]
|
Fig. 1. Chest wall reconstructed with CCP mesh in combination with CFRP strut: the strut was first anchored to two sections of ribs, and then the mesh was sutured with surrounding tissue.
|
|
Postoperatively, the tracheal tube was removed when the dog recovered spontaneous breathing. Prophylactic antibiotics (1,600,000 U of procaine penicillin and 80,000 U of gentamicin sulfate a day) were given postoperatively and maintained for 6 days. The chest tube and subcutaneous drainage was kept for 2–6 days according to the drainage amount, while suction was carried out intermittently with a water seal apparatus.
Paradoxical movement was inspected throughout the observation course, chest X-ray films at 8 weeks and CT photograph at 16 weeks were obtained. One dog with CCP mesh was observed for 8 weeks, one dog of each group for 16 weeks, and the other dogs for 24 weeks. After each observation period, dogs were sacrificed by intravenous administration of sodium pentobarbital. The regenerated chest wall including prosthesis, ribs, and surrounding tissue was removed and analyzed for infection, distortion of original shape, seroma, and adhesions. Samples were further assessed for inflammatory response and cellular infiltration by conventional hematoxylin and eosin (H&E) histology and then examined using a transmission electron microscope (TEM).
|
3. Results
|
|---|
3.1 Observations
All dogs survived the operative procedure and the tracheal tube was removed without respiratory problems. Postoperative inspection revealed a minor paradoxical movement during respiration at the site of reconstruction in dogs with CCP mesh and PP mesh, which had no clinical implications and diminished gradually within 6–8 weeks. Better short-term stabilization was achieved in dogs repaired by CCP mesh in combination with CFRP strut, in which paradoxical movement was barely visible. At 8 weeks postoperatively, the chest wall was firm and the rigidity was satisfactory in all dogs. The long-term stabilization was excellent, with a good esthetic effect, in all the cases observed for 24 weeks.
At 12 weeks postoperatively, one of the dogs with CCP mesh had a mild wound infection and developed a small fistula, which healed spontaneously 4 weeks later after excreting some secretion and several nonabsorbable suture knots without functional consequences. Seromas developed in one dog with polypropylene mesh, which recovered within 3 weeks postoperatively. Postoperative chest roentgenograms and CT scanning showed correct position of the prostheses in all animals with acceptable results (Fig. 2
).
3.2 Gross examination
The CCP mesh prosthesis was found completely incorporated with the fibrous tissue at 8 weeks postoperatively; and the tissue/mesh integration structure was firmly attached to the surrounding tissue. At 16 weeks, only some reticular remnants of the CCP mesh could be detected. The 24-week specimens showed complete absorption of the prosthesis, which was substituted by a thick layer of firm and dense connective tissue, ranging from 2 to 4 mm in thickness (Fig. 3
). At 16 and 24 weeks, examination revealed dense fibrous connective tissue surrounding CFRP strut, which was firmly attached to the two sections of rib stumps. There was no displacement of the strut implants in all four cases at sacrifice. The polypropylene mesh was covered with a thick continuous ingrowing granulation tissue layer, and some slight crimping and plication of the graft was found in both specimens at 16 and 24 weeks postoperatively. All specimens contained adhesions to the underlying lung, which were limited and could be split more easily by blunt dissection in dogs with CCP mesh than dogs with polypropylene mesh.
View larger version (117K):
[in this window]
[in a new window]
|
Fig. 3. Pleural side of regenerative chest wall 24 weeks after reconstruction with CCP mesh shows smooth surface.
|
|
3.3 Microscopy
Microscopic examination revealed that CCP mesh became incorporated with fibrous connective tissue by 8 weeks postoperatively. The entire wall of the porous mesh was infiltrated with fibroblasts, some chronic inflammatory cells (mainly lymphocytes and monocytes), and abundance of blood vessels (Fig. 4
). Newly formed collagen fiber was present in the surrounding tissue. By 16 weeks of implantation, only small remnants of the mesh could be found and inflammation had subsided. At 24 weeks, the CCP mesh grafts disappeared, the original defect was completely filled with dense connective tissue. Aggregates of large multinuclear giant cells were present while plenty of collagenous fiber bands, which were moderately compacted, were concentrated in the connective tissue at the reconstructive site (Fig. 5
). CFRP was encapsulated by a fibrous tissue with a mild tissue reaction (Fig. 6
).
View larger version (158K):
[in this window]
[in a new window]
|
Fig. 4. Photomicrograph revealed that CCP mesh is well incorporated with fibrous connective tissue at 8 weeks postoperatively (hematoxylin and eosin; original magnification, x100).
|
|
View larger version (167K):
[in this window]
[in a new window]
|
Fig. 5. TEM micrograph (CCP mesh 24 weeks after operation). Note: numerous phagosomes ( ) containing degradable polydioxanone particle. The bar present 0.5 µm.
|
|
View larger version (122K):
[in this window]
[in a new window]
|
Fig. 6. CFRP strut was encapsulated with a fibrous layer at 24 weeks postoperatively (hematoxylin and eosin; original magnification, x100).
|
|
|
4. Comment
|
|---|
The management of actual chest wall defects requires a thorough understanding of respiratory mechanics and physiology, and differences of opinion exist about when to provide skeletal reconstruction and what type of reconstruction should be done [1,2]. The current suggestion is to reconstruct all full-thickness skeletal defects that have the potential for producing a physiologic flail and/or a compromise in breathing mechanics [1,8]. The goals of chest wall reconstruction are to restore stability, avoiding paradoxical movements during respiration, obliterate underlying dead space or cavities, provide coverage, protect intrathoracic organs, and maintain or restore esthetic appearance.
Theoretically, autogenous tissues seem to be the most suitable method for reconstruction of chest wall because they allow immediate restoration of a defect without any problem of biological tolerance [9]. However, several disadvantages limit their use: increased surgical trauma and time, possible inadequacy of autologous material, and pain and/or instability at the donor site. Nowadays generally, prosthetic materials are preferred for providing better stability with shorter and simpler surgical procedure. Several authors have shown that stabilization of the chest wall in addition to soft tissue coverage reduced ventilator dependence and overall hospital stay and improved postoperative PaO2 and pulmonary function compared with soft tissue coverage alone. Reconstructive surgeons have relied more and more on the use of prosthetic materials in the past 20 years [2,8].
The ideal material has been sought since prosthetic materials for chest wall reconstruction were first introduced in the 1950s. Historically, numerous materials have been used including alloplastic materials such as stainless steel, titanium, and fiberglass; synthetic materials such as polypropylene (Marlex, Prolene) mesh, Vicryl mesh, polytetrafluoroethylene (Gore-Tex, Teflon) patch, polyethylene, polyester, nylon, silicone, lucite, acrylic, silastic, and methyl methacrylate. However, no single product possesses all the properties of the ideal mesh and most of them were abolished because of all sorts of shortcomings. The choice of prosthetic material, which is based on the surgeon's experience and personal preference, is still difficult and is, to some extent, confusing [2].
Traditionally, most of the available chest wall prosthesis materials are evolved from implanted devices used in the other field such as abdominal repair. A common feature of these materials was their biological ‘inertness’, nonreactivity and durability [10]. According to these principles, several meshes have gained acceptance. Prolene and Marlex mesh were advocated because they provided good semi-rigid skeletal support when sutured under tension fixation and are well incorporated with tissue [11], whereas PTFE often is preferred to Marlex for some surgeons because of its good rigidity, stretchability, conformability, and impermeability. However, the use of these materials is not totally devoid of complications, the most common being infection. Weyant et al. [8] report 12 of 209 patients (5.8%) with prosthesis reconstruction had wound infection. McKenna et al. [12] observed partial infection of Marlex mesh in 25% of their patients. Other long-term complications including chronic and persistent pain, erosion, bleeding, hematoma may occur due to inadequate incorporation, mesh shrinkage and migration. In such circumstances, most of the prostheses must be removed [8]. In addition, the prosthesis will result in pulmonary restrictive disease and scoliosis with growth in children [13].
In the past 20 years, the field of biomaterials began to shift in emphasis from achieving exclusively a bioinert tissue response to instead producing bioactive components that could elicit a controlled action and reaction in the physiological environment [10]. In fact, unlike the abdominal repair with a risk of recurrence, it is not necessary for chest wall prostheses to exist permanently. Primary importance of the prosthesis reconstruction is the establishment of a rigid skeletal structure which is necessary for the dynamic stability of the chest, preserving physiological pulmonary function and, ultimately, for the recovery of the patient, especially in the early postoperative course. Once recovered from the resection and the healing process completed, persistence of the prosthesis seems not to bring benefit to the patient because complications related to its presence are always possible.
We believe that ideal prosthetic material characteristics should (a) be strong enough to withstand physiologic stresses over a long period of time, (b) conform to the chest wall, (c) promote strong host tissue ingrowth, which mimics normal tissue healing and ensuring wall incorporation; (d) resist erosions into surrounding tissue and visceral structures; (e) not induce allergic or adverse foreign body reactions; (f) resist infection; and (g) be easy to use [5,6,14,15].
In our study, CCP mesh proved to be favorable for chest wall reconstruction. Coated with collagen and chitosan, the knitted mesh is more like a PTFE patch in the operation. It is easier to manipulate; it has good rigidity, which has the added benefit of minimizing flailing of the defect; and it could achieve a watertight seal of the pleural space. After the absorption of collagen, the fabric becomes a proper scaffold for cell attachment and fibroblastic proliferation. The monofilament meshes, knitted with polydioxanone, offer the advantages of high tensile strength and resistance to bacterial attachment. It attains strength in the chest for more than 8 weeks and is completely resorbed within 24 weeks, as we observed. This is enough time to allow a fibrous tissue to grow through the prosthesis and to ensure the healing process to be completed. In the gradual process of degradation, the absorbable material might stimulate a moderate inflammatory activity and an extreme formation of connective tissue, which increases the chest wall stiffness [14]. Consequently, the degradation rate and the resulting mechanical features of polydioxanone are incapable of guaranteeing mechanical stability during the maturation of the connective tissues. After complete absorption, the mesh is entirely replaced by a thick collagen-rich connective tissue, sufficient to provide stability to the chest wall and protection to intrathoracic organs. Another advantage of absorbable mesh is that it may be placed in contaminated fields and there is no need to remove it in the presence of infection, as we observed and other studies stated [16].
For patients undergoing extensive chest wall resections, a rigid support is usually used, alone or in combination with mesh material, to provide chest wall stability and to avoid prolonged intubation [17]. However, rigid materials such as struts and plates of metal, and polymethylmethacrylate are too rigid to adjust the size according to defect during the operation and are poorly incorporated with the tissue. The unnecessary rigidity of these materials can create erosion and destruction of adjacent structures with the respiratory movements [9]. The combined use of methyl methacrylate with Marlex mesh partially solves these problems, whereas concerns remain regarding late restriction in view of the rigidity of this substitute and there may be an increased risk of infection due to the large amount of foreign material [8]. Macedo-Neto et al.'s [18] study suggest that methyl methacrylate induces more important mechanical modifications than the PTFE patch, thus significantly higher interference with chest wall dynamic mobility.
As a rigid support, the CFRP seems to be more suitable for chest wall reconstruction than conventional rigid materials. The absorbable composite can be cut according to the defect size with pliers or scissors and can be molded to the desired curve with hot water. The proper toughness and tenacity of the composite ensures the prosthesis does not interfere with chest wall mobility and dynamics while offering enough chest wall stability. The CFRP material keeps its tensile strength for a long time after surgery and has an advantage of lower reactivity [19] than other short-term reabsorbable copolymer such as poly-L-lactide (PLA). Matsui et al. [5] reported removal of the PLA strut was necessitated because of overgrowth of granulation tissue due to the acceleration of the liberation of lactate monomer. This material can be used with other materials to achieve chest wall closure. We believe that this bioresorbable composite is a good addition to other available methods to reconstruct the chest wall in cases where structural integrity is necessary.
|
References
|
|---|
- Mansour KA, Thourani VH, Losken A, Reeves JG, Miller Jr. JI, Carlson GW, Jones GE. Chest wall resections and reconstruction: a 25-year experience. Ann Thorac Surg 2002;73(6):1720-1725[Discussion 1725–6].[Abstract/Free Full Text]
- Arnold PG, Pairolero PC. Chest-wall reconstruction: an account of 500 consecutive patients. Plast Reconstr Surg 1996;98(5):804-810.[Medline]
- Deschamps C, Tirnaksiz BM, Darbandi R, Trastek VF, Allen MS, Miller DL, Arnold PG, Pairolero PC. Early and long-term results of prosthetic chest wall reconstruction. J Thorac Cardiovasc Surg 1999;117(3):588-591[Discussion 591–2].[Abstract/Free Full Text]
- Kroll SS, Walsh G, Ryan B, King RC. Risks and benefits of using Marlex mesh in chest wall reconstruction. Ann Plast Surg 1993;31(4):303-306.[CrossRef][Medline]
- Matsui T, Kitano M, Nakamura T, Shimizu Y, Hyon SH, Ikada Y. Bioabsorbable struts made from poly-L-lactide and their application for treatment of chest deformity. J Thorac Cardiovasc Surg 1994;108(1):162-168.[Abstract/Free Full Text]
- Puma F, Ragusa M, Daddi G. Chest wall stabilization with synthetic reabsorbable material. Ann Thorac Surg 1992;53(3):408-411.[Abstract]
- Yang A, Wu R. Mechanical properties and interfacial interaction of a novel bioabsorbable chitin fiber reinforced polycaprolactone composite. J Mater Sci Lett 2001;20(11):977-979.[CrossRef]
- Weyant MJ, Bains MS, Venkatraman E, Downey RJ, Park BJ, Flores RM, Rizk N, Rusch VW. Results of chest wall resection and reconstruction with and without rigid prosthesis. Ann Thorac Surg 2006;81(1):279-285.[Abstract/Free Full Text]
- Tuncozgur B, Elbeyli L, Gungor A, I
ik F, Akay H. Chest wall reconstruction with autologas rib grafts in dogs and report of a clinic case. Eur J Cardiothorac Surg 1999;16(3):292-295.[Abstract/Free Full Text] - Hench LL, Polak JM. Third-generation biomedical materials. Science 2002;295(5557):1014-1017.[Abstract/Free Full Text]
- Losken A, Thourani VH, Carlson GW, Jones GE, Culbertson JH, Miller JI, Mansour KA. A reconstructive algorithm for plastic surgery following extensive chest wall resection. Br J Plast Surg 2004;57(4):295-302.[CrossRef][Medline]
- McKenna Jr. RJ, Mountain CF, McMurtrey MJ, Larson D, Stiles QR. Current techniques for chest wall reconstruction: expanded possibilities for treatment. Ann Thorac Surg 1988;46(5):508-512.[Abstract]
- Soyer T, Karnak I, Ciftci AO,
enocak ME, Tanyel FC, Büyükpamukçu N. The results of surgical treatment of chest wall tumors in childhood. Pediatr Surg Int 2006;22(2):135-139.[CrossRef][Medline] - Klinge U, Schumpelick V, Klosterhalfen B. Functional assessment and tissue response of short- and long-term absorbable surgical meshes. Biomaterials 2001;22(11):1415-1424.[CrossRef][Medline]
- Rudolphy VJ, Tukkie R, Klopper PJ. Chest wall reconstruction with degradable processed sheep dermal collagen in dogs. Ann Thorac Surg 1991;52(4):821-825.[Abstract]
- van Geel AN, Contant CM, Wiggers T. Full thickness resection of radiation-induced ulcers of the chest wall: reconstruction with absorbable implants, pedicled omentoplasty, and split skin graft. Eur J Surg 1998;164(4):305-307.[CrossRef][Medline]
- Puma F, Avenia N, Ricci F, Guiducci A, Fornasari V, Daddi G. Bone heterograft for chest wall reconstruction after sternal resection. Ann Thorac Surg 1996;61(2):525-529.[Abstract/Free Full Text]
- Macedo-Neto AV, Santos LV, Menezes SL, Paiva DS, Rocco PR, Zin WA. Respiratory mechanics after prosthetic reconstruction of the chest wall in normal rats. Chest 1998;113(6):1667-1672.[CrossRef][Medline]
- Duan L, Xu Zf, Sun K, Zhao Xw, Gong Zy, Qin X. Degradation performance of chitin short fiber reinforced polycaprolactone composite in vivo. Chin J Exp Surg 2005;22(09):1089-1090.
Top
Abstract
1. Introduction
