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ASAIO Journal:
doi: 10.1097/MAT.0b013e3180616b5d
Tissue Engineering

Tracheal Replacements: Part 1

Kucera, Kristin A.*; Doss, Amy E.*; Dunn, Sarah S.*; Clemson, Lindsey A.†; Zwischenberger, Joseph B.*

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From the *Department of Surgery, University of Texas Medical Branch, Galveston, Texas; †Department of Otolaryngology, Emory University, Atlanta, Georgia, U.S.A.

Submitted for consideration October 2006; accepted for publication in revised form March 2007.

Reprint Requests: Joseph B. Zwischenberger, MD, Department of Surgery, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555, U.S.A.

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In this review, we summarize the history of tracheal reconstruction and replacement as well as progress in current tracheal substitutes. In Part 1, we cover the historical highlights of grafts, flaps, tube construction, and tissue transplants and address the progress made in tracheal stenting as a means of temporary tracheal support. This is followed in Part 2 by an analysis of solid and porous tracheal prostheses in experimental and clinical trials. We conclude Part 2 with a summary of recent efforts toward generating a bioengineered trachea. Finally, we provide an algorithm on the spectrum of options available for tracheal replacement.

The need for a prosthetic tracheal replacement is constantly modified by improved surgical techniques for tracheal resection with primary reconstruction. Recent knowledge of tracheal blood supply, mobilization and anastomotic techniques, tolerance of tension, and local tissue reinforcement, as well as postural effects, impacts significantly on the lengths of primary resection/reconstruction. Extensive lesions, such as neoplasms or stenosis, that are longer than half the trachea in adults, or one third the trachea in children, may require prostheses. The spectrum of tracheal replacements ranges from autologous tissue flaps and patches to synthetic stents and prostheses to tissue engineered scaffolding. The goals for a tracheal replacement, as proposed by Belsey1 50 years ago, are (1) a laterally rigid but longitudinally flexible tube, and (2) a surface of ciliated respiratory epithelium. Patients can, however, clear secretions by cough regardless of the conduit surface, decreasing the necessity of the second requirement.

As for artificial prosthetics, as with all artificial organs, the foreign materials should be biocompatible, nontoxic, nonimmunogenic, and noncarcinogenic.2,3 Ideally, these materials should provide or facilitate epithelial resurfacing and not dislocate or erode over time. Tracheal replacements should avoid stenosis and accumulation of secretions and resist bacterial colonization.

To date, no evidence-based clinical trials or clearly superior technology for tracheal replacement has emerged. This review will therefore discuss the techniques and current progress in tracheal replacement and will identify future challenges in the development of tracheal substitutes. In Part 1, we cover the historical highlights of grafts, flaps, tube construction, and tissue transplants and address the progress made in tracheal stenting as a means of temporary tracheal support. This is followed in Part 2 by an analysis of solid and porous tracheal prostheses in experimental and clinical trials as well as a summary of recent efforts toward generating a bioengineered trachea. Finally, we provide an algorithm (Figure 1) on the spectrum of options available for tracheal replacement.

Figure 1
Figure 1
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Tracheal Reconstruction

The optimal method of tracheal reconstruction for a defect <50% of the tracheal length is by circumferential resection and end-to-end anastomosis.4 To facilitate tensionless closure of the tracheal defect, cervical neck flexion can add up to 6 cm. Other methods to add length include extreme transcervical mobilization of the trachea and mainstem bronchi and the suprahyoid laryngeal release. Both provide 1.0–2.0 cm while minimizing the swallowing difficulties of other release procedures. Transthoracic mobilization of the right hilus with division of the pulmonary ligament, intrapericardial dissection of pulmonary vessels, and division of intracartilaginous tracheal ligament allows an additional 3–4 cm length. Combined cervicomediastinal approach may be required for stenosis >5–6 cm, if stenosis is within the thoracic inlet, or if adequate mobilization is not achieved with a cervical approach.1,5–7 The length of resectable trachea varies with age, posture, body habitus, and degree of tracheal pathology.

The Z-plasty technique from plastic surgery has been utilized in noncancerous long tracheal lesions to extend the remaining trachea without breaking epithelial continuity. This technique reduces tension and provides an irregular, but nonetheless continuous, sheet of ciliated epithelium for evacuation of secretions. Foreign material or tissue grafts are used to cover the window defect; however, problems with infection of the patches has limited the use of Z-plasty clinically.8

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Autogenous Grafts With and Without Foreign Material

Tracheal reconstruction, for which primary end-to-end anastomosis cannot be performed, remains an unsolved clinical problem. So far, tracheal replacement approaches have included the use of autologous tissue, autografts, allografts, prosthetic materials, and tissue-engineered trachea, singly or in combination. Unfortunately, limited success has been achieved experimentally and clinically due to anastomotic stenosis, immunologic rejection, local infections, prosthetic dislocation, and material failure.

Various outcomes from using autogenous tissue as patches or in tubular form such as fascia lata,9–12 tracheal wall,9 pericardium,13–15 periosteum with omental wrap,16,17 bone strips with fibrocollagen,18 periosteal patch applied to staggered intercartilaginous relaxing incisions,8 buccal mucosa and auricular cartilage,19 jejunal patches with microvascular reconstruction,20 rib and ear perichondrium,21 nasal cartilage with attached mucosa,22 bronchial patch,23 epidermis,24,25 free fascial graft,26 auricular27 and costal28 cartilage, indicate that small defects can be successfully treated with graft repairs. More recent clinical examples use autogenous tissue such as bronchial patches, dermal grafts, pericardium, and aortic grafts (Table 1). New experimental studies and case reports causing excitement because of their success include Martinod's29,30 use of a thoracic aortic patch with temporary stenting in sheep and his finding of aortic tissue metaplasia into well-differentiated tracheal tissue, including a mucociliary epithelium and regular rings of newly formed cartilage, and Dodge-Khatami's31 use of a carotid artery patch in children both point to future discoveries. Artificial materials used to maintain a rigid wall and support autogenous tissue grafts include: diced cartilage against wire mesh and glass cylinders,32 dermal grafts with wire,33 fascia with tantalum mesh,5,34 tantalum tube,35 Marlex mesh, pericardium with Marlex,13 cartilage and perichondrial strips with silicone stents,36 costal cartilage with polyethylene stents,37 dura mater with wire,38 bladder mucosa with silicone elastomer or polyurethane stents,39,40 fascia lata with coils of steel wire,1,41 fascial flap with polytetrafluoroethylene.42 These foreign materials may be used to prevent collapse of the lumen while various autogenous tissue grafts grow across the partial defects. Associated complications with foreign material were mostly related to lack of biocompatibility and included local infection, anastomotic dehiscence, vascular erosion, granulomatous lesions, and stenosis (Table 2).

Table 1
Table 1
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Table 2
Table 2
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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

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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.

Table 3
Table 3
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Autogenous Tube Construction

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).

Table 4
Table 4
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Tracheal Transplants

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.

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Vascularized Grafts.

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.

Table 5
Table 5
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Tracheal Stents

Although the idea for airway stenting can be dated back to the 1800s,93 the technology to use stenting for airway lesions (obstruction, stenosis, etc.) emerged only in the last 50 years. Harkins used a metal alloy tube to treat a patient with benign tracheal stenosis in 1952,94 and in the 1960s, Montgomery developed a silicon T-shaped prosthesis, the Montgomery T-tube, as a tracheal stent.95 The major problem was finding a material that would not lead to infection or foreign body reaction and could be placed with minimal trauma and complications. The ideal stent needs to fit securely in the airway lumen without requiring external fixation and without causing mucosal injury.96 Satisfactory expansion of the stricture must occur regardless of the origin or the forces causing extrinsic compression, be resistant to extrinsic compression, and allow manipulation in case of obstruction from tumor overgrowth or secretions.96,97 The formation of granulation tissue secondary to airway inflammation should be minimal, and surrounding vascular and cartilaginous structures should not be damaged.

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.

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Silicone Tube Stents

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

Table 6
Table 6
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Expandable Metallic Stents

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.

Table 7
Table 7
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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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