Tracheal transplantation is also being explored but the need for lifelong immunosuppression may inadvertently interfere with tumor disease. Recent experimental studies reported a diminished need for immunosuppression after implantation of grafts pretreated with cryopreservation9,43 or irradiation.32
Autologous tissue reconstruction is always preferable to alloplastic materials. Although tissue grafts can successfully regenerate partial tracheal defects, circumferential or large defects require blood supply and mucosal lining for expectoration. The advantages of flap tissue over graft materials are the independence of its blood supply and its reliability in terms of wound healing. Flap surgery can be done to irradiated or heavily scarred areas, where grafting techniques have little chance to be successful.
Local, regional, and distant free flaps have been reported for experimental tracheal reconstruction, and usually some skeletal element is added. Experiments in vascularized autogenous tissue repair include local skin flaps,44 pedicled intercostal muscle patch,45 pedicled periosteum,16 pedicled bronchus,46 rib and pleural transfer with microvascular anastomosis.47 Tissues from nearly every part of the body have been utilized in an attempt to find the best tissue for tracheal replacement. Examples include a successful multistage procedure using buccal mucosa in beagles,44 omental grafts connected to the esophagus requiring stent placement,48 and mucochondrial composite using vascularization from the thyroid gland.49 A stented tubed radial forearm flap failed with exuberant granulation tissue and stricture formation, but allograft tracheoplasty with radial forearm free flap resulted in nonstenotic trachea.42,50,51 Although experimental autogenous tissue flaps have successfully supported short segments of tracheal reconstruction, the lengthy multistage procedure creates a process not feasible in the situation of cancer treatment.
Clinically, cutaneous chondromucosal forearm tubular flaps, compound tracheal segments vascularized by sternocleidomastoid muscle, deltopectoral flap with costal cartilage and palatal mucosal grafts, and pectoralis major myocutaneous flap with costal cartilage all allowed nonstenotic successful airways; however, all procedures require lengthy multiple stages (Table 3). Yu et al.52 used a radial forearm free flap with polymex mesh and hemishield vascular graft creating a nonstented airway with normal swallowing and voice. Although vascularized autogenous tissue flaps have overall produced successful results with patent, nonstenotic airway, the limiting factor in nearly every procedure remains the complexity and multistage requirement limiting the practicality of the procedure.
The cervical trachea has been experimentally created by formation of a cutaneous trough supported by cartilage rings with staged closure of the trough assisted by tubed pedicle flap from the upper chest wall.34,53,54 Other animal experiments include microvascular jejunal transfer with a cartilage skeleton, series of bilateral hemi rings of cartilage carved from costal arch vascularized by pectoral flap, muscle and flaps stiffened with cartilage and lined with skin around a stent, and rib perichondrium around silicone rods. All procedures resulted in difficult or negative outcomes.34,55–59 Clinically, tube construction has been successfully completed by Edgerton, Serrano, and Zhao34,55,60; however, all procedures were multistage difficult procedures used as a last resort (Table 4).
The first report of tracheal autografts in 1918 reported successful transfer of 3–9 segments in half of the subjects. Orthotopic transplantation of tracheal tissue was most often unsuccessful, because blood supply to the transplanted tissue was too slow to prevent necrosis or stenosis. In autografts of very short segments the animals survived; however, the cartilage was absorbed and converted to fibrous tissue.61 Longer segments resulted in dissolution, stenosis, and obstruction due to loss of blood supply.62 Multiple experiments concluded survival with devascularized autografts is poor with only minimal success using short segments.62–65 Tracheal allografts mostly met with failure due to rejection.65–68 However, even with immunosuppression the allografts failed with abundance of fibrous tissue.9,34,62,63,69 Very short grafts resulted in minor fibrous tissue to complete fibrous stenosis.4,62,65,70–72 Although allografts of partial tracheal wall prevented lumen obstruction, even these grafts were replaced by flaccid scars.73 Studies by Beigel et al.66 concluded tracheal transplants carry antigens and have immunogenic action from the donor; Bujia et al.67 supported these results reporting the mucosa of the human trachea is the major antigenic source. Because of these failures, attempts were made to preserve the tissue and remove antigenic sources. Experiments involved partly de-epithelializing, merthiolate-treating, and cold-preserving canine allografts. Preserving solutions include Tyrode's solution, 4% formaldehyde, alcohol, saline, or lyophilization at −4°C.2,32,65,74–77 The results from these attempts were uniform failures with fibrosis, stenosis, or necrosis the usual outcome.
Autografts can be directly vascularized by anastomoses or with pedicled flaps. Early attempts at tracheal allotransplantation achieved patent airways, and although omental transplants promoted early revascularization, experiments to minimize postsurgical complications continued (Table 5).123–125 Indirect vascularization using omentopexy could sustain short tracheal segments and promoted quicker revascularization, but the omentum is not sufficient to support long tracheal grafts nor chondrocytes.78–83 Yokomise et al.84 prevented central graft necrosis by introducing an autograft split in the middle by an omental circumferential insertion. The grafts revascularized without stenosis or necrosis. Murai et al.85 removed the cartilage rings before transplantation to increase omental contact resulting in improved blood supply and reepithelialization. Fresh allografts with omental revascularization without immunosuppression failed due to rejection81,83,86–89; however, cryopreserved allografts with omental flap revascularization survived without immunosuppression.84,86,87 Cryopreservation inhibits allogenicity while structural integrity appears to be maintained. Cryopreservation of allografts reduces acute rejection and permits early revascularization, but chronic rejection leads to vascular occlusion and atrophy.86,89,90 Direct revascularization of grafts concluded mixed results. Composite thyrotracheal graft vascularized by thyroid artery anastomosed to the common carotid without immunosuppression preserved cartilage, but tracheal soft tissue necrosed. All tissues survived with immunosuppression from cyclosporine and hydrocortisone.91 Daly et al.92 anastomosed the largest bronchial artery in a patch of descending aorta to the recipient left internal thoracic artery with excellent airway healing without dehiscence or granulation tissue of trachea.
Endotracheal/bronchial stenting may open large airways severely narrowed or obstructed due to a tumor mass, when the patient is not a candidate for surgical treatment, primary radiation, or chemotherapy, or when those therapies are not likely to be effective alone.96 Other tracheobronchial disorders requiring stents include complications from tracheostomy, postintubation injuries (such as subglottic stenosis), benign tracheal stenosis (for nonsurgical candidates, patients refractory to bronchoscopic resection or dilatation, or pending response to systemic therapy or surgical resection), tracheobronchomalacia, anastomotic strictures after lung and heart-lung transplantation, or tracheo- or broncho-esophageal fistula.97,98
There are two main types of stents in use today—silicone tube stents and expandable metallic stents. We will primarily focus on stents which have the potential to serve as tracheal replacements.
The Montgomery T-tube, the first of the silicone stents, remains important in the treatment of subglottic stenosis or obstruction. It serves as both an upper tracheal stent and tracheostomy tube and is inserted through a tracheostomy stoma.96,98 Many versions of the Montgomery T-tube have been developed over the years, including one by Westaby et al.99 with a long distal branch that bifurcates at the carina.96,98 An endoscopically placed, modified Silastic T-tube stent was used by Cooper et al.100 in patients with malignant tracheobronchial obstruction. The horizontal limb was pulled out through a tracheostomy stoma much like the Montgomery T-tube.98
The Dumon stent (Bryan Corp, Woburn, MA) is a silicone tube stent that has external studs at regular intervals to prevent problems with stent migration and dislodgement. These stents have proven to have excellent clinical outcomes when placed in lower trachea or bronchi.101,102 The Dynamic stent (Rüsch, AG Kernan, Germany) is a silicone Y-stent with a long tracheal and left main bronchial limb, short right bronchial limb, metallic ring-reinforced anterolateral walls, and a collapsible posterior wall that mimics the dynamics of the membranous trachea during respiration.103
The main advantages of using silicone stents are their removability, unreactivity, adjustability, resistance to tumor ingrowth, and minimal granulation tissue formation.98,104 Silicone stents are also easily customized to fit the airway anatomy of any patient and have a defined, fixed diameter that prevents uncontrolled expansion.104 Limitations of using silicone stents include difficult placement; tendency to dislodge, distort, or migrate resulting in need for revision or replacement; lack of tissue ingrowth and epithelization; obstruction from secretion accumulation; and the need for rigid bronchoscopy and general anesthesia for placement.98,104 Also, these stents have a lower inner-to-outer diameter ratio compared with metallic stents, which contributes to stent obstruction from secretions. See Table 6 for specific details.98
The successful use of expandable metallic stents in the vascular and biliary systems has led to their use in the treatment of benign and malignant airway stenoses.98 The Gianturco stent, a first-generation expandable metallic stent, allows delivery via a catheter into vascular or airway stenoses.105,106 Available in fixed lengths (2 or 2.5 cm), tandem stents have also been constructed. The Palmaz stent is a fixed-diameter, balloon-expandable, stainless steel wire mesh tubular stent. Because this stent does not exhibit intrinsic radial force, it is positioned and seated by balloon expansion, and once expanded does not exert continual expanding pressure on the airway; therefore, it theoretically has less risk of hyperexpansion and perforation.98,104
The second generation of expandable metallic stents began with the development of the Wallstent, also known as the Schneider prosthesis. The Wallstent is a self-expandable tubular mesh stent made of braided cobalt-based super alloy monofilaments coated with silicone. It is loaded in a delivery catheter, inserted with flexible fiberoptic bronchoscope under fluoroscopic guidance, and then expands to the preset diameter.98 Commonly used in Europe for airway stenoses, the Wallstent has excellent flexibility and conformance to the patient's airway, is easily adaptable, and effectively treats pure extrinsic compression and esophagobronchial fistulas.96 However, the Wallstent has significant problems with tumor and granulation tissue ingrowth that often results in obstruction. A newer version of the Wallstent, the Permalume, is covered by a thin layer of silicone rubber all except the proximal and distal 5 mm, to prevent tumor or granulation tissue ingrowth through the stent. The Wallgraft has the same construction as the Wallstent and Permalume except it is completely covered by polyethylene.104
The latest version of the Wallstent is the Ultraflex stent, a self-expandable stent made of woven single strand nitinol (nickel-titanium alloy) that allows for easier endoscopic retrieval. Uniquely, the nickel-titanium alloy has “shape-memory,” meaning that at low temperatures it deforms plastically (martensitic state) and at high temperatures it regains its original shape (austenitic state).107 For placement of these stents, a guidewire is inserted via rigid bronchoscope and positioned fluoroscopically under general anesthesia. The stents are inserted on a loaded delivery catheter that is advanced over the guidewire until it is radiographically aligned with previously placed skin markers identifying the limits of the lesion.108,109
The smooth and studded Polyflex stents are newly available options for expandable metallic stents. Polyflex stents are self-expandable silicone-covered polyester wire mesh stents designed to prevent tumor ingrowth via the internal silicone coating.
Advantages of the more permanent expandable metallic stents over silicone tube stents include easier delivery and placement via flexible bronchoscope and fluoroscopic guidance under local anesthesia, higher internal-to-external diameter ratio, less obstruction from secretions, improved stability, decreased migration, and ability to accommodate to multiple tracheal dimensions.98,104 These types of stents are also particularly useful in patients with intense extrinsic compression or large areas of obstruction or stenosis. Uncovered metallic stents, theoretically, have improved epithelization and incorporation into the surrounding tracheal tissue.104 Covered stents have the advantage of decreased tumor or granulation tissue ingrowth and improved removability. However, the uncovered bare metal ends still have the potential for tumor ingrowth or granulation tissue.104
The permanence and, therefore, decreased adjustability and removability are among the primary disadvantages to using expandable metallic stents. This is particularly problematic for patients with benign tracheal stenosis or when tumor ingrowth or granulation tissue causes stent obstruction necessitating repeat debridement or re-stenting.98,104 The need for fluoroscopy and potential for erosion into surrounding structures with possible bronchovascular fistulas are less favorable aspects of expandable metallic stents.104 See Table 7 for specific details of these stents.
The management of tracheal defects for which primary end-to-end anastomosis cannot be performed remains a clinical challenge. To date, the use of tissue flaps, autografts, allografts, prosthetic materials, stents, or a combination of these methods has met with limited clinical significance due to a multitude of complications. We have constructed an algorithm to show the extent of the current and potential options available for tracheal replacement (Figure 1). Fortunately, the emergence of tissue engineering has prompted exploration into tracheal substitutes that may provide more successful replacement options in the near future.
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