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Reconstruction of the Trachea Sydney Ch’ng, MBBS, PhD, FRACS1,2 Gerald L. Wong, MBChB, MHM, FCICM, FANZCA3 Jonathan R. Clark, MBBS (Hon), MBiostat, FRACS1 1 Department of Head and Neck Surgery, Royal Prince Alfred Hospital,
Sydney, New South Wales, Australia 2 Department of Plastic Surgery, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia 3 Department of Anesthesia, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia
Address for correspondence Sydney Ch’ng, MBBS, PhD, FRACS, Department of Head and Neck Surgery, Royal Prince Alfred Hospital, P O Box M182, Missenden Road Post Office, Sydney, NSW 2050, Australia (e-mail: [email protected]).
Abstract
Keywords
► ► ► ► ►
trachea autologous prosthesis bioengineering transplantation
This article reviews established methods of autologous tracheal reconstruction, the various synthetic prostheses that have been used in clinical practice, and briefly describes the latest developments in stem cell tracheal bioengineering and allogeneic tracheal transplantation. Reconstruction of the trachea is challenging due to its part cervical part thoracic location, proximity to major vessels, variable blood supply, and its constant colonization with bacteria. In cases of limited resection, primary anastomosis, autologous patch grafts, local advancement rotation flaps, and locoregional cutaneous and muscle flaps will often suffice. In more extensive resections, complex composite microsurgical reconstruction with a radial forearm free flap with cartilage grafts for skeletal support has proven to be viable and reliable. Synthetic tracheal prostheses, solid as well as porous, have been trialed with disappointing results. Infection, dislodgement, migration, and obstruction are not uncommon. Reconstruction with the cadaveric tracheal allografts and aortic allografts continue to be fraught with complications, specifically graft infections. Tracheal bioengineering and tracheal allotransplantation have emerged relatively recently. Despite early promising results, long-term outcome data on these new techniques are still lacking.
The field of tracheal reconstruction has experienced impressive progress. In the 1950s, primary tracheal anastomosis was thought to be unachievable beyond segmental excision of 2 cm.1 Primary anastomosis up to 4 cm, complex tracheoplasty and microvascular composite free flap reconstruction for curative procedures, and endoluminal (laser) ablation and stenting for symptomatic relief or palliative intent are now mainstream procedures. Relatively recently, the trachea joined the ever expanding list of transplantable allogeneic organs and vascularized composite allografts; and clinical trials for stem cell bioengineering for tracheal reconstruction are underway.2,3 Tracheal resection and reconstruction, however, remain fraught with difficulties. Major surgery on the trachea is
challenging due to several inherent factors. It is partly cervical and partly thoracic in location crossing the confined space of the thoracic inlet. Different surgical approaches, including an anterior cervical approach with/without median sternotomy or a thoracotomy for more distal airway access may be warranted depending on location of the lesion. The trachea is closely associated with major vessels, larynx, esophagus, pulmonary ligaments, and bronchi. Catastrophic hemorrhage and mediastinal sepsis are potentially lethal complications. The respiratory epithelium is bacteria colonized; and the trachea is constantly mobile with respiration and neck motion, and subjected to forces caused by coughing, sneezing, and straining, all contributing to the limited success with synthetic scaffolds and stents in the long term. It
received June 18, 2013 accepted after revision August 27, 2013 published online December 12, 2013
Copyright © 2014 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.
DOI http://dx.doi.org/ 10.1055/s-0033-1358786. ISSN 0743-684X.
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lacks a major named vascular pedicle, but instead carries a tenuous segmental blood supply. This has major implications for tracheoplasty especially in irradiated subjects and is the main obstacle to direct revascularization in tracheal allotransplantation. This article reviews tried and tested methods of autologous (primarily cervical) tracheal reconstruction, briefly describes various synthetic prostheses that have been used with variable success rates, and provides an overview on allogeneic tracheal transplantation and stem cell bioengineering (►Table 1).
Anatomy The trachea extends from the inferior border of cricoid to the carinal spur. It is on average 11.8 cm (range, 10–13 cm) in length. It is formed by a series of 18 to 22 C-shaped cartilaginous rings (with intervening fibrous membrane) that are deficient posteriorly, where membranous trachea or trachealis bridges the gap. Its lumen is oval shaped in cross section, measuring 1.8 cm in the anteroposterior dimension and 2.3 cm in the lateral dimension. The trachea is relatively superficial just below the cricoid but slopes
posteriorly as it enters the mediastinum at the level of the sternal notch. The anterior surface of the cervical trachea is covered from cephalad to caudad, by the isthmus of the thyroid gland, the inferior thyroid veins, the arteria thyroidea ima (when present), and paired sternohyoid and sternothyroid muscles enveloped in a pretracheal layer of cervical fascia. Superiorly, the pretracheal fascia is attached to the thyroid and cricoid cartilages and inferiorly fuses with the pericardium. The posterior wall of the trachea, composed of trachealis muscle and connective tissue, lies against the esophagus. Lateral to the cervical trachea are the common carotid arteries, the lobes of the thyroid gland, parathyroid glands, recurrent laryngeal nerves, branches of the inferior thyroid artery, and the brachiocephalic trunk crosses anterior to the trachea to branch on the right side.4 The thoracic trachea lies in the superior mediastinum. On the anterior surface, lies the arch of the aorta, the inferior thyroid and left brachiocephalic veins, remnants of the thymus, and the manubrium with sternohyoid and sternothyroid attached. Anterolaterally on the left, are the left common carotid and subclavian arteries, and the right vagus nerve and azygos vein on the right.4
Table 1 Comparison of reconstructive techniques Reconstruction method
Advantages
Disadvantages
Autologous reconstruction Primary anastomosis/autologous grafts/locoregional flaps
Locoregional flaps provide reliable reinforcement to anastomosis
Primary anastomosis limited to (generally) segmental defects of a maximum of 6 tracheal rings in nonradiated neck, and 4 in irradiated neck Autografts limited to small defects
Microvascular free flap reconstruction
Viable option for large composite defects with cartilage grafts added/ implanted during prefabrication Keratinizing skin paddle compatible as epithelial lining for trachea
Donor site morbidity
Prosthesis
Ready availability
Complications with infection, dislodgement, migration, stenosis, and vascular erosion Permanent—removal will cause collapse of trachea
Cadaveric allograft
Viable option for long-segmental and complex defects
Avascularity—complications with infection
Aortic allograft
Lacking in rigidity—need for permanent stenting Complications with infection/tracheoesophageal fistula Progressive contraction of graft
Tracheal bioengineering
Viable option for long-segmental and complex defects No immunosuppression required
Unpredictable mechanical and functional properties of tracheal scaffold following decellularization (human trachea) Requires specialized bioreactor
Tracheal allotransplantation (with prefabrication)
Viable option for long-segmental and complex defects Identifiable vascular pedicle
Immunosuppression Additional surgery required to access remote region for implantation of allograft Long duration of prefabrication
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The upper trachea receives its primary blood supply from branches of the inferior thyroid artery in a variable pattern. Furthermore, distally in the lower trachea, this is supplemented by contribution from the bronchial arteries, and to a lesser extent, the subclavian, internal mammary, innominate, and supreme intercostal arteries. Venous drainage is by networks located mainly in mucosa, submucosa, and tunica adventitia. These venous plexuses, situated around trachea and esophagus, ultimately drain into the inferior thyroid venous plexus. 5 The pattern of blood supply is therefore primarily segmental and approaches the trachea laterally.
Relationship with the Recurrent Laryngeal Nerve The recurrent laryngeal nerves course posterolaterally to the trachea in the groove between the trachea and esophagus, and enter the larynx deep to cricopharyngeus immediately posterior to the cricothyroid joint and inferior cornua of the thyroid cartilage.
Anesthesia and Airway Management Meticulous preoperative evaluation and discussion between anesthesiology and surgical teams is required to plan airway management in these cases. Options for induction include maintenance of spontaneous ventilation or positive pressure ventilation (including jet ventilation) depending on the tracheal pathology. 6,7 A range of airway equipment must be available including video laryngoscopes, fiberoptic, and rigid bronchoscopes (including pediatric sizes). Intubation may require smaller endotracheal tubes, microlaryngeal tubes, wire-reinforced tubes, or tracheostomy tubes.7–9 Maintenance of anesthesia with an intravenous technique ensures drug delivery and avoids environmental contamination.7,8 Maintenance of ventilation when the trachea has been transected is via surgically placed tubes (endotracheal or endobronchial), or jet ventilation, for example, via a rigid bronchoscope or airway catheter.6,7 Extracorporeal techniques, including cardiopulmonary bypass, oxygenation, or carbon dioxide removal, have been used in some cases where ventilation has not been possible, although is associated with its own risks, particularly bleeding.6,7 Intraoperative goals include careful fluid balance, normothermia, adequate analgesia using systemic or regional techniques, minimizing use of long-acting sedatives, and prevention of postoperative nausea and vomiting.6,8,9 Important considerations during emergence and extubation include maintenance of neck flexion, assessment of tracheal patency and bleeding, and assessment of laryngeal edema and vocal cord function.10 Early extubation is generally desired to prevent the endotracheal tube and positive pressure ventilation from affecting the surgical site.9 However, reintubation in this cohort is often extremely challenging.6,10
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Autologous Tracheal Reconstruction Primary Anastomosis and Advancement Rotation Flap For most patients undergoing segmental excision, a maximum of 6 tracheal rings (4 cm) can be resected and anastomosed primarily with acceptable tension in a nonirradiated trachea with neck flexion and transcervical mobilization.11 Mobilization is performed with blunt dissection in the avascular plane just anterior to the trachea and deep to the innominate artery down to the level of the carina. In contrast, freeing of the membranous wall of the trachea from the esophagus on the posterior aspect will not greatly increase mobility, and hence circumferential dissection is only made at the level of the lesion that is to be excised. The lateral blood supply must not be injured to prevent later trachea necrosis and stenosis.12,13 When the length of resection prohibits direct anastomosis with these simple maneuvers, the suprahyoid release can be used to allow the trachea to devolve more distally for additional relaxation. A short transverse incision over the hyoid is performed dividing stylohyoid, mylohyoid, geniohyoid, and hyoglossus.14 The resultant descent of the laryngeal framework does unfortunately cause difficulties with swallowing and aspiration, although most patients recover with time and assistance.13 For resection greater than 5 to 6 cm, located within the thoracic inlet, or if adequate mobilization cannot be achieved with a cervical anterior approach alone, a combined cervicomediastinal approach may be required with the addition of division of the pulmonary ligament, intrapericardial dissection of pulmonary vessels, and division of intracartilaginous tracheal ligament.15,16 Anastomosis is typically commenced at the posterior membranous wall, from midline to lateral with sutures placed laterally through the cartilaginous rings to take tension off the anastomosis. The posterior wall, that is, trachealis, does not need to be resected to complete a segmental excision if oncologically uninvolved. It can be concertinaed into a blind pouch in the tracheal anastomosis (►Fig. 1).11 A more conservative approach is required in an irradiated trachea where segmental excision of 4 rings is probably the maximum limit for which a primary anastomosis can be performed. Buttressing of the anastomosis with a regional
Fig. 1 Trachealis in the posterior wall of trachea can be left unresected in segmental resection if uninvolved with tumor. Trachealis is concertinaed into a blind pouch in primary anastomosis (, asterisk) (C, cricoid). Adapted from Ch’ng et al. 11 Journal of Reconstructive Microsurgery
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or free flap is prudent in cases where a segmental resection is performed in the setting of previous radiotherapy.11 Several options are available for noncircumferential resection. For a limited defect localized anteriorly or laterally, a tracheal flap can be fashioned to even out tension across a wider surface (►Fig. 2). For larger eccentric defects (> 6 rings), an option is to convert the defect into an asymmetrical segmental defect and to primarily anastomose the trachea with rotation of the distal trachea without excision of the remaining trachea (►Fig. 3).11
Autologous Grafts Autologous tissue, as patches or in tubular form, such as fascia lata, pericardium, pleura, periosteum, aorta, bone strips with fibrocollagen, periosteal patch, rib and ear perichondrium, dermis, auricular, and costal cartilage have been used with variable success in small defects.17–26 Larger defects, however, require reconstruction with an independent blood supply for more predictable outcomes.
Locoregional Cutaneous and Muscle Flaps Locoregional cutaneous and muscle flaps are useful in tracheal reconstruction for several reasons. They provide reinforcement for the anastomotic line and are especially important in the setting of previous (chemo)radiation. They can also function to obliterate any dead space, and to interpose between the trachea and innominate artery (or any exposed major vascular structure) to prevent the oftenfatal complication of a tracheoinnominate fistula.11,27 In cases where restoration of structural integrity is not required, they can be used to patch the tracheal defect.11 Depending on the specific requirements, some common workhorse flaps include the strap muscles, sternocleidomastoid, internal mammary artery perforator flap, pectoralis major, deltopectoral, and latissimus dorsi.11,28,29 For larger and more complex defects, the flap may be prefabricated with cartilage graft for skeletal support and/or mucosal/skin graft for lining.17,30
Microvascular Free Tissue Reconstruction Various reports have shown that microvascular free flap reconstruction is a viable option that can be customized to large composite defects, and that keratinizing skin is compatible as epithelial lining within the tracheal lumen.11,31–35
Fig. 2 Large lateral defect reconstructed with an advancement rotation tracheal flap based laterally. Adapted from Ch’ng et al. 11 Journal of Reconstructive Microsurgery
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Fig. 3 In reconstructing a large eccentric defect, configuration of the defect can be drastically changed by disconnecting the distal trachea, and rotating and advancing the distal segment cephalad for anastomosis. Adapted from Ch’ng et al. 11
Teng et al described a prefabricated radial forearm free flap for tracheal reconstruction in a 53-year-old woman who developed critical airway stenosis 2.5 years following chemoradiation for a T4N2c squamous cell carcinoma of the hypopharynx.34 In an attempt to widen her laryngeal airway, a thyrotracheal autograft (a segment of hemitrachea based on the thyroid gland as vascular carrier) was transferred cephalad.34,36 This created a 8-cm secondary defect inferiorly that involved 40% of the anterior tracheal circumference. Prefabrication of a radial forearm free flap was performed 2 months later, where curved strips of costal cartilage were implanted in the subcutaneous layer of a planned radial forearm harvest site. The flap was raised 4 weeks later and inset with the forearm skin turned in as tracheal lining. A second deltopectoral flap was added to provide anterior cervical skin coverage. The patient was successfully decannulated from her tracheostomy 2 weeks later. She unfortunately suffered from chronic aspiration and was unable to tolerate oral intake despite intensive swallowing therapy. She eventually opted for a total laryngectomy.34 Fujiwara et al and Olias et al have described similar techniques of two- and three-stage prefabricated radial forearm free flap tracheal reconstruction.32,35 Ch’ng et al presented three cases of radial forearm free flap in a series of 15 cases of oncologic tracheal reconstruction. Two radial forearm free flaps were fashioned to buttress relatively high-tension primary and advancement rotation flap anastomoses, respectively, and the other was suspended to longitudinal cartilage strut grafts bridging a circumferential defect in a
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Tracheal Reconstruction single-staged reconstruction (►Fig. 4). Two of these patients sustained minor air leaks that did not require surgical intervention. No other complications were encountered at a mean follow-up period of 17 months. One was extubated at the end of surgery, and the other two successfully decannulated from their Montgomery T-tube (Boston Medical Products Inc., Westborough, MA) subsequently.11 Yu et al reported seven cases of large tracheal defects reconstructed with radial forearm free flap combined with a
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variety of prosthetic materials, including Hemashield vascular graft (Boston Scientific, Natrick, MA), polytetrafluoroethylene (PTFE) ring vascular graft, and porous highdensity polyethylene for semirigid support. Major complications in their series included air leak in four patients, exposure and removal of prosthesis in two patients, and cardiopulmonary complications in two patients. One patient died from multiorgan failure 2 months postoperatively, whereas two out of the remaining six patients remained tracheostomy dependent at last follow-up (5 years) and death (1 year), respectively.31
Tracheal Prostheses A variety of solid and porous prostheses have been trialed clinically.
Since solid prostheses fail to become well integrated with the surrounding tissue, problems with infection, dislodgement, migration, and obstruction commonly develop.37,38 In addition, a solid tube is a permanent prosthesis because its removal will cause the connective tissue tract that has formed around it to collapse, contract, and obstruct. Materials that have been trialed clinically in occasional cases include stainless steel, silicone, polythene (polyethylene), PTFE, polyethylene and tantalum, and Lucite.39–47 In an attempt to reduce granulation formation and to encourage fixation, Neville et al used a silicone prosthesis with suturable subterminal fabric cuffs that were intussuscepted into the tracheal ends.43 Disappointingly, the prosthesis was found to cause obstructive granulation tissue, migration, and vascular erosion.42 Solid prostheses, despite some success for a varied period of time, all eventually tend to fail. Successful surgical prostheses in other sites, for example, vascular conduits, heart valves, and orthopedic devices, are all implanted in potentially sterile mesenchymal tissues. The respiratory epithelium, on the contrary, is chronically colonized by bacteria.37,48
Porous Prosthesis
Fig. 4 (a) Large anterior defect () following excision of recurrent papillary thyroid carcinoma with a focus of anaplastic thyroid carcinoma in an irradiated trachea. Part of the cricoid (C) was resected with the tumor specimen. The common carotid artery (CCA) was skeletonized in resection of the tumor (I, innominate artery). (b) Cartilage struts (black arrow) were used to bridge the defect to add rigidity to the reconstruction. (c) A radial forearm free flap (white arrow) was used to reconstruct the defect. A sternocleidomastoid flap (black arrow) was fashioned to separate the carotid artery from the reconstructed trachea and the innominate artery. Adapted from Ch’ng et al.11
The disappointment with impervious solid prostheses prompted the search for porous materials that would permit ingrowth of host connective tissue, bridging of regenerative epithelium, and incorporation into the native tracheal wall. Scherer et al worked out that the minimal porosity required of mesh prostheses for capillary ingrowth is 40 to 60 μm.49 Wire, plastic rings, or coils have been incorporated into these meshes for increased rigidity, whereas polymer coatings or autologous tissue reinforcement, for example, omentum, fascia, and pericardium have been applied to decrease the complication of air leaks.38 Steel wire, tantalum covered with fascia lata, skin and tantalum gauze, heavy Marlex with or without pericardial covering, Ivalon and wire, and PTFE have been used in clinical settings as patches or tubes.17,31,39,50–54 The overall outcome has been disappointing. Some degree of mesh incorporation commonly takes place, but the simultaneous proliferation of scar tissue often leads to obstruction and stenosis. Large segments of mesh often Journal of Reconstructive Microsurgery
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remain uncovered by connective tissue, and bacterial colonization ensues.37 The epithelium generally fails to migrate sufficiently to cover the entire neotracheal lumen, causing granulations, cicatrization, and stenosis to form especially in the center of the prosthesis.55 Fatal complications from erosion of the brachiocephalic artery have been reported for Marlex as well as steel mesh prostheses.39,52,53 Marlex also has a propensity to harbor Pseudomonas aeruginosa, which causes purulent sputum and halitosis.37
ment from dehiscence of allograft and a subclavian/carotid artery blowout. Mean duration of allograft stenting for the group was 0.67 years. Eight of the 10 patients sustained an infection after at least 1 of their allograft surgical procedures. Despite an average of 7.38 additional procedures after allograft placement, including laryngotracheoplasty and slide tracheoplasty, the overall decannulation rate was only 60%.56 Limited success from both studies suggests that cadaveric tracheal allograft should be reserved for when autologous reconstructive techniques have failed.
Cadaveric Allograft The cadaveric tracheal allograft was first introduced by Herberhold in 1979. Processed to have all cells and major histocompatibility markers removed, it is an option for patients with long-segment tracheal stenosis or recurrent stenosis.56 Jacobs et al reviewed both the North American and the total worldwide pediatric experience with cadaveric allograft reconstruction as treatment for patients with long-segment and recurrent tracheal stenosis. The anterior cartilage is resected preserving the posterior tracheal wall or trachealis. Chemically preserved cadaveric trachea is inset after placement of a silicone intraluminal stent. Six patients (three children and three adults) in North America, and more than 100 adults and 31 children worldwide have undergone this reconstructive technique. There was one fatality in North America from a tracheoinnominate fistula hemorrhage. Worldwide, 26 of the 31 pediatric patients survived (follow-up 5 months to 14 years), and only 1 of the 26 children remained tracheostomy dependent.57 Recently, Propst et al presented their experience of 14 cadaveric tracheal allograft reconstructions in 10 children. Mean allograft length was 60% of the total recipient trachea. There was one death within a few weeks of allograft place-
Aortic Allografts Wurtz et al reported their experience with the use of fresh and cryopreserved aortic allografts in six patients with extensive (range, 5.5–11 cm) mucoepidermoid and adenoid cystic carcinomas, at a median follow-up period of 34 months.58 Tracheal resection was followed by interposition of the graft splinted by a silicone stent. All grafts were wrapped with a pectoral muscle flap, with/without an additional thymopericardial fat flap (►Fig. 5). No immunosuppressive therapy was administered. One patient developed acute anterior spinal cord ischemia, the reason for which remained unclear. Another sustained partial graft necrosis from invasive Candida albicans infection, and required regrafting on day 18. Three patients developed tracheoesophageal fistula, including one who died of massive hemoptysis following failed fistula repair. Stent removal has not been attempted in any patient. No acute or chronic graft rejection has been detected. On endoscopic examinations, focal epithelialization and sparse calcifications suggestive of osseous metaplasia within the graft have been noted. The strength afforded by the osseous metaplasia, if any, was dubious. Furthermore, there was progressive contraction of the graft (mean 28% at 6
Fig. 5 (a) Diagram showing aortic allograft and intraluminal stenting in place. (b) Operative view of tracheal reconstruction with fresh aortic allograft in place (IA, innominate artery; AA, aortic allograft). (c) Operative view of interposition of the pectoral muscle flap between the graft and large vessels (IA, innominate artery; AO, aorta). Adapted from Wurtz et al. 58
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months), which warranted serial endoscopic stent shortening/replacement.
Tracheal Bioengineering Alternative methods of tracheal reconstruction for longsegmental defects have surfaced due to the inconsistent and unsatisfactory outcomes from various synthetic prostheses and decellularized allografts, including bioengineered tracheas and tracheal allotransplantation. Macchiarini et al in 2008 reported transplanting a decellularized human donor trachea, colonized with the recipient’s epithelial cells, and mesenchymal stem cell-derived chondrocytes into a 30-year-old woman with bronchomalacia. One month postoperatively, three-dimensional computed tomography scans showed a widely patent tissue-engineered trachea-reconstructed left main bronchus. Lung function tests done at 2 months postoperatively were within the normal range for age and sex, and no antidonor HLA antibodies were detected on serology despite no immunosuppressive therapy.59 The main criticism of this procedure was the lack of restoration of blood flow to the allograft, hence questionable applicability to a major tracheal defect, although laser-Doppler readings at 4 months confirmed the presence of a microvasculature.59,60 The recipient eventually needed stenting of her collapsed airway several months later and has had several stent insertions and removals in the last 5 years.61 In an attempt to address the disadvantages associated with a decellularized human donor trachea, including shortage of donor organs, potential immunogenicity from donor proteins, unpredictability in mechanical and functional properties of the tracheal scaffold following decellularization, and excessive costs, a bioartificial nanocomposite was developed by the same group.59,62 A 36-year-old man with recurrent primary trachea cancer received a custom-made Y-shaped nanocomposite conduit previously seeded with autologous bone marrow mononuclear cells by incubation in a bioreactor for 36 hours. An omental flap was wrapped around the construct. At 5 months, the nanocomposite trachea was reported to be well integrated with the native adjacent tissue with patent anastomoses, and partly covered by nearly healthy epithelium. Macchiarini et al have since treated 14 more patients with decellularized/reseeded tracheas and stem cell-seeded bioartificial nanocomposite scaffolds, including three children. At least two of these patients have died under circumstances that might be related to their implants. Although recently the recipient of major grants to commence human clinical trials, Macchiarini et al have been criticized for failure to provide detailed and long-term data on these patients.61
Tracheal Allotransplantation Rose et al reported the first allogeneic tracheal transplantation in 1979. The trachea was first implanted heterotopically in the recipient’s sternocleidomastoid muscle before being transferred to the orthotopic position 3 weeks later. The
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patient was not given immunosuppressive therapy. Satisfying results with no rejection, infection, or ischemia were reported after 9 weeks, but no further information was provided on long-term outcome.63 In 1993, Levashov et al described a case of one-stage distal trachea transplantation where the omentum was wrapped around the allograft. The 24-year-old woman recipient with idiopathic fibrosing mediastinitis developed early rejection and then progressive stenosis, which became problematic enough to require stenting. Whether the tracheal allograft or the underlying disease progression was the cause of the stenosis was unclear.64 In 2004, Klepetko et al described heterotopic tracheal allotransplantation and omentum wrapping in the abdomen of an end-stage chronic obstructive pulmonary disease patient who received bilateral lung transplant from the same donor. The tracheal transplant was ultimately not required and was explanted after a total of 60 days in the abdomen, and on analysis, found to be mechanically intact and viable.65 Delaere et al described successful tracheal transplantation after heterotopic revascularization of the allograft in a recipient’s forearm fascia. Once revascularization was achieved, the mucosal lining of the graft was replaced progressively with buccal mucosa from the recipient. The tracheal chimera eventually consisted of respiratory epithelium from the donor and buccal mucosa from the recipient. The patient’s pulmonary function tests 1 year after cessation of immunosuppressive therapy showed no significant functional upper airway obstruction.60 The available literature supports tracheal allotransplantation as a viable option for treating long-segment tracheal defects, albeit not without challenges and not always successful.59–61,63–66 The trachea lacks an identifiable vascular pedicle that would allow direct anastomosis to the recipient’s vessels in the neck. Restoration of reliable arterial inflow and venous outflow to the tracheal allograft therefore remains a major challenge. Heterotopic indirect vascularization is time-consuming, and requires additional surgery to another anatomical region for implantation of the allograft. Although there has been serendipitous discovery of immune tolerance in a small fraction of transplant recipients, allografts typically requires nonspecific immunosuppressive therapy to prevent transplant rejection. Immunosuppressive therapy predisposes to opportunistic infections, malignancies, metabolic imbalances, and end-organ damage.2
Conclusion Primary anastomosis, complex tracheoplasties, and microvascular free flap reconstruction for the trachea are now established techniques. The ideal synthetic prosthesis, however, remains elusive. Although human allograft transplantation and stem-cell engineering seem promising, few patients have been described (most treated on “compassionate” grounds), follow-up is short, and the equipment is expensive and not readily available. Despite impressive advances in tracheal reconstruction, to achieve a laterally rigid, Journal of Reconstructive Microsurgery
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longitudinally flexible, epithelialized, well-integrated, nonimmunogenic, reliable, and durable reconstruction for longsegment tracheal defects continues to be challenging.
25 Ohlsén L, Nordin U. Tracheal reconstruction with perichondrial
grafts. Scand J Plast Reconstr Surg 1976;10(2):135–145 26 Azorin JF, Bertin F, Martinod E, Laskar M. Tracheal replacement
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with an aortic autograft. Eur J Cardiothorac Surg 2006;29(2): 261–263 Panje WR, Herberhold C, eds. Head and Neck Surgery, vol 3. New York, NY: Thieme Medical Publishers; 1995 Ris HB, Krueger T, Cheng C, Pasche P, Monnier P, Magnusson L. Tracheo-carinal reconstructions using extrathoracic muscle flaps. Eur J Cardiothorac Surg 2008;33(2):276–283 Iyer NG, Clark JR, Ashford BG. Internal mammary artery perforator flap for head and neck reconstruction. ANZ J Surg 2009;79(11): 799–803 Shinohara H, Yuzuriha S, Matsuo K, Kushima H, Kondoh S. Tracheal reconstruction with a prefabricated deltopectoral flap combined with costal cartilage graft and palatal mucosal graft. Ann Plast Surg 2004;53(3):278–281 Yu P, Clayman GL, Walsh GL. Long-term outcomes of microsurgical reconstruction for large tracheal defects. Cancer 2011;117(4): 802–808 Fujiwara T, Nishino K, Numajiri T. Tracheal reconstruction with a prefabricated and double-folded radial forearm free flap. J Plast Reconstr Aesthet Surg 2009;62(6):790–794 Kashiwa K, Kobayashi S, Tono H, Nohara T, Honda T, Sakurai S. Reconstruction of the cervical trachea using a prefabricated corticoperiosteal flap from the femur. Ann Plast Surg 2009; 62(6):633–636 Teng MS, Malkin BD, Urken ML. Prefabricated composite free flaps for tracheal reconstruction: a new technique. Ann Otol Rhinol Laryngol 2005;114(11):822–826 Olias J, Millán G, da Costa D. Circumferential tracheal reconstruction for the functional treatment of airway compromise. Laryngoscope 2005;115(1):159–161 Zur KB, Urken ML. Vascularized hemitracheal autograft for laryngotracheal reconstruction: a new surgical technique based on the thyroid gland as a vascular carrier. Laryngoscope 2003;113(9): 1494–1498 Grillo HC. Tracheal replacement: a critical review. Ann Thorac Surg 2002;73(6):1995–2004 Doss AE, Dunn SS, Kucera KA, Clemson LA, Zwischenberger JB. Tracheal replacements: Part 2. ASAIO J 2007;53(5):631–639 Beattie EJ Jr, Blades B, Keshishian JM. Tracheal reconstruction. J Thorac Surg 1956;32(6):707–725, discussion, 725–727 Jarvis FJ. Pulmonary resection in the treatment of pulmonary tuberculosis. A study of 100 consecutive cases. West J Surg Obstet Gynecol 1950;58(11):643–647 Cotton BH, Hills B, Penido JR. Resection of the trachea for carcinoma; report of two cases. J Thorac Surg 1952;24(3): 231–245 Toomes H, Mickisch G, Vogt-Moykopf I. Experiences with prosthetic reconstruction of the trachea and bifurcation. Thorax 1985; 40(1):32–37 Neville WE, Bolanowski JP, Kotia GG. Clinical experience with the silicone tracheal prosthesis. J Thorac Cardiovasc Surg 1990;99(4): 604–612, discussion 612–613 Kramish D, Morfit HM. The use of a Teflon prosthesis to bridge complete sleeve defects in the human trachea. Am J Surg 1963; 106:704–708 Ekestrom S, Carlens E. Teflon prosthesis in tracheal defects in man. Acta Chir Scand Suppl 1959(245):71–75 McCall JW, Whitaker CW. The use of prostheses in the larynx and trachea. A preliminary report. Trans Am Laryngol Assoc 1962; 83:16–24 Longmire WP Jr. The repair of large defects of the trachea. Ann Otol Rhinol Laryngol 1948;57(3):875–883 Rich JT, Gullane PJ. Current concepts in tracheal reconstruction. Curr Opin Otolaryngol Head Neck Surg 2012;20(4):246–253
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thetic reconstruction of the trachea. Arch Otorhinolaryngol 1986; 243(4):215–223 Cahan WG. Carcinoma of intrathoracic trachea: excision and repair by tantalum gauze-fascia lata graft; report of a case. J Thorac Surg 1952;23(5):513–527 Yeh TJ, Batayias G, Peters H, Ellison RG. Metastatic carcinoma to the trachea: report of a case of palliation by resection and Marlex graft. J Thorac Cardiovasc Surg 1965;49:886–892 Moghissi K. Reconstruction of trachea with Marlex mesh pericardium following circumferential excision. J R Coll Surg Edinb 1975; 20(5):327–331 Pearson FG, Henderson RD, Gross AE, Ginsberg RJ, Stone RM. The reconstruction of circumferential tracheal defects with a porous prosthesis. An experimental and clinical study using heavy Marlex mesh. J Thorac Cardiovasc Surg 1968;55(5):605–616 Nelson RJ, Goldberg L, White RA, Shors E, Hirose FM. Neovascularity of a tracheal prosthesis/tissue complex. J Thorac Cardiovasc Surg 1983;86(6):800–808 Grillo HC. Surgery of the trachea. Curr Probl Surg 1970;(Jul):3–59 Propst EJ, Prager JD, Meinzen-Derr J, Clark SL, Cotton RT, Rutter MJ. Pediatric tracheal reconstruction using cadaveric homograft. Arch Otolaryngol Head Neck Surg 2011;137(6):583–590 Jacobs JP, Quintessenza JA, Andrews T, et al. Tracheal allograft reconstruction: the total North American and worldwide pediatric experiences. Ann Thorac Surg 1999;68(3):1043–1051, discussion 1052 Wurtz A, Porte H, Conti M, et al. Surgical technique and results of tracheal and carinal replacement with aortic allografts for salivary
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gland-type carcinoma. J Thorac Cardiovasc Surg 2010;140(2): 387–393, e2 Macchiarini P, Jungebluth P, Go T, et al. Clinical transplantation of a tissue-engineered airway. Lancet 2008;372(9655): 2023–2030 Delaere P, Vranckx J, Verleden G, De Leyn P, Van Raemdonck D; Leuven Tracheal Transplant Group. Tracheal allotransplantation after withdrawal of immunosuppressive therapy. N Engl J Med 2010;362(2):138–145 Vogel G. Trachea transplants test the limits. Science 2013; 340(6130):266–268 Jungebluth P, Alici E, Baiguera S, et al. Tracheobronchial transplantation with a stem-cell-seeded bioartificial nanocomposite: a proof-of-concept study. Lancet 2011;378(9808):1997–2004 Rose KG, Sesterhenn K, Wustrow F. Tracheal allotransplantation in man. Lancet 1979;1(8113):433 Levashov YuN, Yablonsky PK, Cherny SM, Orlov SV, Shafirovsky BB, Kuznetzov IM. One-stage allotransplantation of thoracic segment of the trachea in a patient with idiopathic fibrosing mediastinitis and marked tracheal stenosis. Eur J Cardiothorac Surg 1993;7(7): 383–386 Klepetko W, Marta GM, Wisser W, et al. Heterotopic tracheal transplantation with omentum wrapping in the abdominal position preserves functional and structural integrity of a human tracheal allograft. J Thorac Cardiovasc Surg 2004; 127(3):862–867 Elliott MJ, De Coppi P, Speggiorin S, et al. Stem-cell-based, tissue engineered tracheal replacement in a child: a 2-year follow-up study. Lancet 2012;380(9846):994–1000
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Reconstruction of the Trachea Sydney Ch’ng, MBBS, PhD, FRACS1,2 Gerald L. Wong, MBChB, MHM, FCICM, FANZCA3 Jonathan R. Clark, MBBS (Hon), MBiostat, FRACS1 1 Department of Head and Neck Surgery, Royal Prince Alfred Hospital,
Sydney, New South Wales, Australia 2 Department of Plastic Surgery, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia 3 Department of Anesthesia, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia
Address for correspondence Sydney Ch’ng, MBBS, PhD, FRACS, Department of Head and Neck Surgery, Royal Prince Alfred Hospital, P O Box M182, Missenden Road Post Office, Sydney, NSW 2050, Australia (e-mail: [email protected]).
Abstract
Keywords
► ► ► ► ►
trachea autologous prosthesis bioengineering transplantation
This article reviews established methods of autologous tracheal reconstruction, the various synthetic prostheses that have been used in clinical practice, and briefly describes the latest developments in stem cell tracheal bioengineering and allogeneic tracheal transplantation. Reconstruction of the trachea is challenging due to its part cervical part thoracic location, proximity to major vessels, variable blood supply, and its constant colonization with bacteria. In cases of limited resection, primary anastomosis, autologous patch grafts, local advancement rotation flaps, and locoregional cutaneous and muscle flaps will often suffice. In more extensive resections, complex composite microsurgical reconstruction with a radial forearm free flap with cartilage grafts for skeletal support has proven to be viable and reliable. Synthetic tracheal prostheses, solid as well as porous, have been trialed with disappointing results. Infection, dislodgement, migration, and obstruction are not uncommon. Reconstruction with the cadaveric tracheal allografts and aortic allografts continue to be fraught with complications, specifically graft infections. Tracheal bioengineering and tracheal allotransplantation have emerged relatively recently. Despite early promising results, long-term outcome data on these new techniques are still lacking.
The field of tracheal reconstruction has experienced impressive progress. In the 1950s, primary tracheal anastomosis was thought to be unachievable beyond segmental excision of 2 cm.1 Primary anastomosis up to 4 cm, complex tracheoplasty and microvascular composite free flap reconstruction for curative procedures, and endoluminal (laser) ablation and stenting for symptomatic relief or palliative intent are now mainstream procedures. Relatively recently, the trachea joined the ever expanding list of transplantable allogeneic organs and vascularized composite allografts; and clinical trials for stem cell bioengineering for tracheal reconstruction are underway.2,3 Tracheal resection and reconstruction, however, remain fraught with difficulties. Major surgery on the trachea is
challenging due to several inherent factors. It is partly cervical and partly thoracic in location crossing the confined space of the thoracic inlet. Different surgical approaches, including an anterior cervical approach with/without median sternotomy or a thoracotomy for more distal airway access may be warranted depending on location of the lesion. The trachea is closely associated with major vessels, larynx, esophagus, pulmonary ligaments, and bronchi. Catastrophic hemorrhage and mediastinal sepsis are potentially lethal complications. The respiratory epithelium is bacteria colonized; and the trachea is constantly mobile with respiration and neck motion, and subjected to forces caused by coughing, sneezing, and straining, all contributing to the limited success with synthetic scaffolds and stents in the long term. It
received June 18, 2013 accepted after revision August 27, 2013 published online December 12, 2013
Copyright © 2014 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662.
DOI http://dx.doi.org/ 10.1055/s-0033-1358786. ISSN 0743-684X.
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lacks a major named vascular pedicle, but instead carries a tenuous segmental blood supply. This has major implications for tracheoplasty especially in irradiated subjects and is the main obstacle to direct revascularization in tracheal allotransplantation. This article reviews tried and tested methods of autologous (primarily cervical) tracheal reconstruction, briefly describes various synthetic prostheses that have been used with variable success rates, and provides an overview on allogeneic tracheal transplantation and stem cell bioengineering (►Table 1).
Anatomy The trachea extends from the inferior border of cricoid to the carinal spur. It is on average 11.8 cm (range, 10–13 cm) in length. It is formed by a series of 18 to 22 C-shaped cartilaginous rings (with intervening fibrous membrane) that are deficient posteriorly, where membranous trachea or trachealis bridges the gap. Its lumen is oval shaped in cross section, measuring 1.8 cm in the anteroposterior dimension and 2.3 cm in the lateral dimension. The trachea is relatively superficial just below the cricoid but slopes
posteriorly as it enters the mediastinum at the level of the sternal notch. The anterior surface of the cervical trachea is covered from cephalad to caudad, by the isthmus of the thyroid gland, the inferior thyroid veins, the arteria thyroidea ima (when present), and paired sternohyoid and sternothyroid muscles enveloped in a pretracheal layer of cervical fascia. Superiorly, the pretracheal fascia is attached to the thyroid and cricoid cartilages and inferiorly fuses with the pericardium. The posterior wall of the trachea, composed of trachealis muscle and connective tissue, lies against the esophagus. Lateral to the cervical trachea are the common carotid arteries, the lobes of the thyroid gland, parathyroid glands, recurrent laryngeal nerves, branches of the inferior thyroid artery, and the brachiocephalic trunk crosses anterior to the trachea to branch on the right side.4 The thoracic trachea lies in the superior mediastinum. On the anterior surface, lies the arch of the aorta, the inferior thyroid and left brachiocephalic veins, remnants of the thymus, and the manubrium with sternohyoid and sternothyroid attached. Anterolaterally on the left, are the left common carotid and subclavian arteries, and the right vagus nerve and azygos vein on the right.4
Table 1 Comparison of reconstructive techniques Reconstruction method
Advantages
Disadvantages
Autologous reconstruction Primary anastomosis/autologous grafts/locoregional flaps
Locoregional flaps provide reliable reinforcement to anastomosis
Primary anastomosis limited to (generally) segmental defects of a maximum of 6 tracheal rings in nonradiated neck, and 4 in irradiated neck Autografts limited to small defects
Microvascular free flap reconstruction
Viable option for large composite defects with cartilage grafts added/ implanted during prefabrication Keratinizing skin paddle compatible as epithelial lining for trachea
Donor site morbidity
Prosthesis
Ready availability
Complications with infection, dislodgement, migration, stenosis, and vascular erosion Permanent—removal will cause collapse of trachea
Cadaveric allograft
Viable option for long-segmental and complex defects
Avascularity—complications with infection
Aortic allograft
Lacking in rigidity—need for permanent stenting Complications with infection/tracheoesophageal fistula Progressive contraction of graft
Tracheal bioengineering
Viable option for long-segmental and complex defects No immunosuppression required
Unpredictable mechanical and functional properties of tracheal scaffold following decellularization (human trachea) Requires specialized bioreactor
Tracheal allotransplantation (with prefabrication)
Viable option for long-segmental and complex defects Identifiable vascular pedicle
Immunosuppression Additional surgery required to access remote region for implantation of allograft Long duration of prefabrication
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The upper trachea receives its primary blood supply from branches of the inferior thyroid artery in a variable pattern. Furthermore, distally in the lower trachea, this is supplemented by contribution from the bronchial arteries, and to a lesser extent, the subclavian, internal mammary, innominate, and supreme intercostal arteries. Venous drainage is by networks located mainly in mucosa, submucosa, and tunica adventitia. These venous plexuses, situated around trachea and esophagus, ultimately drain into the inferior thyroid venous plexus. 5 The pattern of blood supply is therefore primarily segmental and approaches the trachea laterally.
Relationship with the Recurrent Laryngeal Nerve The recurrent laryngeal nerves course posterolaterally to the trachea in the groove between the trachea and esophagus, and enter the larynx deep to cricopharyngeus immediately posterior to the cricothyroid joint and inferior cornua of the thyroid cartilage.
Anesthesia and Airway Management Meticulous preoperative evaluation and discussion between anesthesiology and surgical teams is required to plan airway management in these cases. Options for induction include maintenance of spontaneous ventilation or positive pressure ventilation (including jet ventilation) depending on the tracheal pathology. 6,7 A range of airway equipment must be available including video laryngoscopes, fiberoptic, and rigid bronchoscopes (including pediatric sizes). Intubation may require smaller endotracheal tubes, microlaryngeal tubes, wire-reinforced tubes, or tracheostomy tubes.7–9 Maintenance of anesthesia with an intravenous technique ensures drug delivery and avoids environmental contamination.7,8 Maintenance of ventilation when the trachea has been transected is via surgically placed tubes (endotracheal or endobronchial), or jet ventilation, for example, via a rigid bronchoscope or airway catheter.6,7 Extracorporeal techniques, including cardiopulmonary bypass, oxygenation, or carbon dioxide removal, have been used in some cases where ventilation has not been possible, although is associated with its own risks, particularly bleeding.6,7 Intraoperative goals include careful fluid balance, normothermia, adequate analgesia using systemic or regional techniques, minimizing use of long-acting sedatives, and prevention of postoperative nausea and vomiting.6,8,9 Important considerations during emergence and extubation include maintenance of neck flexion, assessment of tracheal patency and bleeding, and assessment of laryngeal edema and vocal cord function.10 Early extubation is generally desired to prevent the endotracheal tube and positive pressure ventilation from affecting the surgical site.9 However, reintubation in this cohort is often extremely challenging.6,10
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Autologous Tracheal Reconstruction Primary Anastomosis and Advancement Rotation Flap For most patients undergoing segmental excision, a maximum of 6 tracheal rings (4 cm) can be resected and anastomosed primarily with acceptable tension in a nonirradiated trachea with neck flexion and transcervical mobilization.11 Mobilization is performed with blunt dissection in the avascular plane just anterior to the trachea and deep to the innominate artery down to the level of the carina. In contrast, freeing of the membranous wall of the trachea from the esophagus on the posterior aspect will not greatly increase mobility, and hence circumferential dissection is only made at the level of the lesion that is to be excised. The lateral blood supply must not be injured to prevent later trachea necrosis and stenosis.12,13 When the length of resection prohibits direct anastomosis with these simple maneuvers, the suprahyoid release can be used to allow the trachea to devolve more distally for additional relaxation. A short transverse incision over the hyoid is performed dividing stylohyoid, mylohyoid, geniohyoid, and hyoglossus.14 The resultant descent of the laryngeal framework does unfortunately cause difficulties with swallowing and aspiration, although most patients recover with time and assistance.13 For resection greater than 5 to 6 cm, located within the thoracic inlet, or if adequate mobilization cannot be achieved with a cervical anterior approach alone, a combined cervicomediastinal approach may be required with the addition of division of the pulmonary ligament, intrapericardial dissection of pulmonary vessels, and division of intracartilaginous tracheal ligament.15,16 Anastomosis is typically commenced at the posterior membranous wall, from midline to lateral with sutures placed laterally through the cartilaginous rings to take tension off the anastomosis. The posterior wall, that is, trachealis, does not need to be resected to complete a segmental excision if oncologically uninvolved. It can be concertinaed into a blind pouch in the tracheal anastomosis (►Fig. 1).11 A more conservative approach is required in an irradiated trachea where segmental excision of 4 rings is probably the maximum limit for which a primary anastomosis can be performed. Buttressing of the anastomosis with a regional
Fig. 1 Trachealis in the posterior wall of trachea can be left unresected in segmental resection if uninvolved with tumor. Trachealis is concertinaed into a blind pouch in primary anastomosis (, asterisk) (C, cricoid). Adapted from Ch’ng et al. 11 Journal of Reconstructive Microsurgery
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or free flap is prudent in cases where a segmental resection is performed in the setting of previous radiotherapy.11 Several options are available for noncircumferential resection. For a limited defect localized anteriorly or laterally, a tracheal flap can be fashioned to even out tension across a wider surface (►Fig. 2). For larger eccentric defects (> 6 rings), an option is to convert the defect into an asymmetrical segmental defect and to primarily anastomose the trachea with rotation of the distal trachea without excision of the remaining trachea (►Fig. 3).11
Autologous Grafts Autologous tissue, as patches or in tubular form, such as fascia lata, pericardium, pleura, periosteum, aorta, bone strips with fibrocollagen, periosteal patch, rib and ear perichondrium, dermis, auricular, and costal cartilage have been used with variable success in small defects.17–26 Larger defects, however, require reconstruction with an independent blood supply for more predictable outcomes.
Locoregional Cutaneous and Muscle Flaps Locoregional cutaneous and muscle flaps are useful in tracheal reconstruction for several reasons. They provide reinforcement for the anastomotic line and are especially important in the setting of previous (chemo)radiation. They can also function to obliterate any dead space, and to interpose between the trachea and innominate artery (or any exposed major vascular structure) to prevent the oftenfatal complication of a tracheoinnominate fistula.11,27 In cases where restoration of structural integrity is not required, they can be used to patch the tracheal defect.11 Depending on the specific requirements, some common workhorse flaps include the strap muscles, sternocleidomastoid, internal mammary artery perforator flap, pectoralis major, deltopectoral, and latissimus dorsi.11,28,29 For larger and more complex defects, the flap may be prefabricated with cartilage graft for skeletal support and/or mucosal/skin graft for lining.17,30
Microvascular Free Tissue Reconstruction Various reports have shown that microvascular free flap reconstruction is a viable option that can be customized to large composite defects, and that keratinizing skin is compatible as epithelial lining within the tracheal lumen.11,31–35
Fig. 2 Large lateral defect reconstructed with an advancement rotation tracheal flap based laterally. Adapted from Ch’ng et al. 11 Journal of Reconstructive Microsurgery
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Fig. 3 In reconstructing a large eccentric defect, configuration of the defect can be drastically changed by disconnecting the distal trachea, and rotating and advancing the distal segment cephalad for anastomosis. Adapted from Ch’ng et al. 11
Teng et al described a prefabricated radial forearm free flap for tracheal reconstruction in a 53-year-old woman who developed critical airway stenosis 2.5 years following chemoradiation for a T4N2c squamous cell carcinoma of the hypopharynx.34 In an attempt to widen her laryngeal airway, a thyrotracheal autograft (a segment of hemitrachea based on the thyroid gland as vascular carrier) was transferred cephalad.34,36 This created a 8-cm secondary defect inferiorly that involved 40% of the anterior tracheal circumference. Prefabrication of a radial forearm free flap was performed 2 months later, where curved strips of costal cartilage were implanted in the subcutaneous layer of a planned radial forearm harvest site. The flap was raised 4 weeks later and inset with the forearm skin turned in as tracheal lining. A second deltopectoral flap was added to provide anterior cervical skin coverage. The patient was successfully decannulated from her tracheostomy 2 weeks later. She unfortunately suffered from chronic aspiration and was unable to tolerate oral intake despite intensive swallowing therapy. She eventually opted for a total laryngectomy.34 Fujiwara et al and Olias et al have described similar techniques of two- and three-stage prefabricated radial forearm free flap tracheal reconstruction.32,35 Ch’ng et al presented three cases of radial forearm free flap in a series of 15 cases of oncologic tracheal reconstruction. Two radial forearm free flaps were fashioned to buttress relatively high-tension primary and advancement rotation flap anastomoses, respectively, and the other was suspended to longitudinal cartilage strut grafts bridging a circumferential defect in a
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Tracheal Reconstruction single-staged reconstruction (►Fig. 4). Two of these patients sustained minor air leaks that did not require surgical intervention. No other complications were encountered at a mean follow-up period of 17 months. One was extubated at the end of surgery, and the other two successfully decannulated from their Montgomery T-tube (Boston Medical Products Inc., Westborough, MA) subsequently.11 Yu et al reported seven cases of large tracheal defects reconstructed with radial forearm free flap combined with a
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variety of prosthetic materials, including Hemashield vascular graft (Boston Scientific, Natrick, MA), polytetrafluoroethylene (PTFE) ring vascular graft, and porous highdensity polyethylene for semirigid support. Major complications in their series included air leak in four patients, exposure and removal of prosthesis in two patients, and cardiopulmonary complications in two patients. One patient died from multiorgan failure 2 months postoperatively, whereas two out of the remaining six patients remained tracheostomy dependent at last follow-up (5 years) and death (1 year), respectively.31
Tracheal Prostheses A variety of solid and porous prostheses have been trialed clinically.
Since solid prostheses fail to become well integrated with the surrounding tissue, problems with infection, dislodgement, migration, and obstruction commonly develop.37,38 In addition, a solid tube is a permanent prosthesis because its removal will cause the connective tissue tract that has formed around it to collapse, contract, and obstruct. Materials that have been trialed clinically in occasional cases include stainless steel, silicone, polythene (polyethylene), PTFE, polyethylene and tantalum, and Lucite.39–47 In an attempt to reduce granulation formation and to encourage fixation, Neville et al used a silicone prosthesis with suturable subterminal fabric cuffs that were intussuscepted into the tracheal ends.43 Disappointingly, the prosthesis was found to cause obstructive granulation tissue, migration, and vascular erosion.42 Solid prostheses, despite some success for a varied period of time, all eventually tend to fail. Successful surgical prostheses in other sites, for example, vascular conduits, heart valves, and orthopedic devices, are all implanted in potentially sterile mesenchymal tissues. The respiratory epithelium, on the contrary, is chronically colonized by bacteria.37,48
Porous Prosthesis
Fig. 4 (a) Large anterior defect () following excision of recurrent papillary thyroid carcinoma with a focus of anaplastic thyroid carcinoma in an irradiated trachea. Part of the cricoid (C) was resected with the tumor specimen. The common carotid artery (CCA) was skeletonized in resection of the tumor (I, innominate artery). (b) Cartilage struts (black arrow) were used to bridge the defect to add rigidity to the reconstruction. (c) A radial forearm free flap (white arrow) was used to reconstruct the defect. A sternocleidomastoid flap (black arrow) was fashioned to separate the carotid artery from the reconstructed trachea and the innominate artery. Adapted from Ch’ng et al.11
The disappointment with impervious solid prostheses prompted the search for porous materials that would permit ingrowth of host connective tissue, bridging of regenerative epithelium, and incorporation into the native tracheal wall. Scherer et al worked out that the minimal porosity required of mesh prostheses for capillary ingrowth is 40 to 60 μm.49 Wire, plastic rings, or coils have been incorporated into these meshes for increased rigidity, whereas polymer coatings or autologous tissue reinforcement, for example, omentum, fascia, and pericardium have been applied to decrease the complication of air leaks.38 Steel wire, tantalum covered with fascia lata, skin and tantalum gauze, heavy Marlex with or without pericardial covering, Ivalon and wire, and PTFE have been used in clinical settings as patches or tubes.17,31,39,50–54 The overall outcome has been disappointing. Some degree of mesh incorporation commonly takes place, but the simultaneous proliferation of scar tissue often leads to obstruction and stenosis. Large segments of mesh often Journal of Reconstructive Microsurgery
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remain uncovered by connective tissue, and bacterial colonization ensues.37 The epithelium generally fails to migrate sufficiently to cover the entire neotracheal lumen, causing granulations, cicatrization, and stenosis to form especially in the center of the prosthesis.55 Fatal complications from erosion of the brachiocephalic artery have been reported for Marlex as well as steel mesh prostheses.39,52,53 Marlex also has a propensity to harbor Pseudomonas aeruginosa, which causes purulent sputum and halitosis.37
ment from dehiscence of allograft and a subclavian/carotid artery blowout. Mean duration of allograft stenting for the group was 0.67 years. Eight of the 10 patients sustained an infection after at least 1 of their allograft surgical procedures. Despite an average of 7.38 additional procedures after allograft placement, including laryngotracheoplasty and slide tracheoplasty, the overall decannulation rate was only 60%.56 Limited success from both studies suggests that cadaveric tracheal allograft should be reserved for when autologous reconstructive techniques have failed.
Cadaveric Allograft The cadaveric tracheal allograft was first introduced by Herberhold in 1979. Processed to have all cells and major histocompatibility markers removed, it is an option for patients with long-segment tracheal stenosis or recurrent stenosis.56 Jacobs et al reviewed both the North American and the total worldwide pediatric experience with cadaveric allograft reconstruction as treatment for patients with long-segment and recurrent tracheal stenosis. The anterior cartilage is resected preserving the posterior tracheal wall or trachealis. Chemically preserved cadaveric trachea is inset after placement of a silicone intraluminal stent. Six patients (three children and three adults) in North America, and more than 100 adults and 31 children worldwide have undergone this reconstructive technique. There was one fatality in North America from a tracheoinnominate fistula hemorrhage. Worldwide, 26 of the 31 pediatric patients survived (follow-up 5 months to 14 years), and only 1 of the 26 children remained tracheostomy dependent.57 Recently, Propst et al presented their experience of 14 cadaveric tracheal allograft reconstructions in 10 children. Mean allograft length was 60% of the total recipient trachea. There was one death within a few weeks of allograft place-
Aortic Allografts Wurtz et al reported their experience with the use of fresh and cryopreserved aortic allografts in six patients with extensive (range, 5.5–11 cm) mucoepidermoid and adenoid cystic carcinomas, at a median follow-up period of 34 months.58 Tracheal resection was followed by interposition of the graft splinted by a silicone stent. All grafts were wrapped with a pectoral muscle flap, with/without an additional thymopericardial fat flap (►Fig. 5). No immunosuppressive therapy was administered. One patient developed acute anterior spinal cord ischemia, the reason for which remained unclear. Another sustained partial graft necrosis from invasive Candida albicans infection, and required regrafting on day 18. Three patients developed tracheoesophageal fistula, including one who died of massive hemoptysis following failed fistula repair. Stent removal has not been attempted in any patient. No acute or chronic graft rejection has been detected. On endoscopic examinations, focal epithelialization and sparse calcifications suggestive of osseous metaplasia within the graft have been noted. The strength afforded by the osseous metaplasia, if any, was dubious. Furthermore, there was progressive contraction of the graft (mean 28% at 6
Fig. 5 (a) Diagram showing aortic allograft and intraluminal stenting in place. (b) Operative view of tracheal reconstruction with fresh aortic allograft in place (IA, innominate artery; AA, aortic allograft). (c) Operative view of interposition of the pectoral muscle flap between the graft and large vessels (IA, innominate artery; AO, aorta). Adapted from Wurtz et al. 58
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months), which warranted serial endoscopic stent shortening/replacement.
Tracheal Bioengineering Alternative methods of tracheal reconstruction for longsegmental defects have surfaced due to the inconsistent and unsatisfactory outcomes from various synthetic prostheses and decellularized allografts, including bioengineered tracheas and tracheal allotransplantation. Macchiarini et al in 2008 reported transplanting a decellularized human donor trachea, colonized with the recipient’s epithelial cells, and mesenchymal stem cell-derived chondrocytes into a 30-year-old woman with bronchomalacia. One month postoperatively, three-dimensional computed tomography scans showed a widely patent tissue-engineered trachea-reconstructed left main bronchus. Lung function tests done at 2 months postoperatively were within the normal range for age and sex, and no antidonor HLA antibodies were detected on serology despite no immunosuppressive therapy.59 The main criticism of this procedure was the lack of restoration of blood flow to the allograft, hence questionable applicability to a major tracheal defect, although laser-Doppler readings at 4 months confirmed the presence of a microvasculature.59,60 The recipient eventually needed stenting of her collapsed airway several months later and has had several stent insertions and removals in the last 5 years.61 In an attempt to address the disadvantages associated with a decellularized human donor trachea, including shortage of donor organs, potential immunogenicity from donor proteins, unpredictability in mechanical and functional properties of the tracheal scaffold following decellularization, and excessive costs, a bioartificial nanocomposite was developed by the same group.59,62 A 36-year-old man with recurrent primary trachea cancer received a custom-made Y-shaped nanocomposite conduit previously seeded with autologous bone marrow mononuclear cells by incubation in a bioreactor for 36 hours. An omental flap was wrapped around the construct. At 5 months, the nanocomposite trachea was reported to be well integrated with the native adjacent tissue with patent anastomoses, and partly covered by nearly healthy epithelium. Macchiarini et al have since treated 14 more patients with decellularized/reseeded tracheas and stem cell-seeded bioartificial nanocomposite scaffolds, including three children. At least two of these patients have died under circumstances that might be related to their implants. Although recently the recipient of major grants to commence human clinical trials, Macchiarini et al have been criticized for failure to provide detailed and long-term data on these patients.61
Tracheal Allotransplantation Rose et al reported the first allogeneic tracheal transplantation in 1979. The trachea was first implanted heterotopically in the recipient’s sternocleidomastoid muscle before being transferred to the orthotopic position 3 weeks later. The
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patient was not given immunosuppressive therapy. Satisfying results with no rejection, infection, or ischemia were reported after 9 weeks, but no further information was provided on long-term outcome.63 In 1993, Levashov et al described a case of one-stage distal trachea transplantation where the omentum was wrapped around the allograft. The 24-year-old woman recipient with idiopathic fibrosing mediastinitis developed early rejection and then progressive stenosis, which became problematic enough to require stenting. Whether the tracheal allograft or the underlying disease progression was the cause of the stenosis was unclear.64 In 2004, Klepetko et al described heterotopic tracheal allotransplantation and omentum wrapping in the abdomen of an end-stage chronic obstructive pulmonary disease patient who received bilateral lung transplant from the same donor. The tracheal transplant was ultimately not required and was explanted after a total of 60 days in the abdomen, and on analysis, found to be mechanically intact and viable.65 Delaere et al described successful tracheal transplantation after heterotopic revascularization of the allograft in a recipient’s forearm fascia. Once revascularization was achieved, the mucosal lining of the graft was replaced progressively with buccal mucosa from the recipient. The tracheal chimera eventually consisted of respiratory epithelium from the donor and buccal mucosa from the recipient. The patient’s pulmonary function tests 1 year after cessation of immunosuppressive therapy showed no significant functional upper airway obstruction.60 The available literature supports tracheal allotransplantation as a viable option for treating long-segment tracheal defects, albeit not without challenges and not always successful.59–61,63–66 The trachea lacks an identifiable vascular pedicle that would allow direct anastomosis to the recipient’s vessels in the neck. Restoration of reliable arterial inflow and venous outflow to the tracheal allograft therefore remains a major challenge. Heterotopic indirect vascularization is time-consuming, and requires additional surgery to another anatomical region for implantation of the allograft. Although there has been serendipitous discovery of immune tolerance in a small fraction of transplant recipients, allografts typically requires nonspecific immunosuppressive therapy to prevent transplant rejection. Immunosuppressive therapy predisposes to opportunistic infections, malignancies, metabolic imbalances, and end-organ damage.2
Conclusion Primary anastomosis, complex tracheoplasties, and microvascular free flap reconstruction for the trachea are now established techniques. The ideal synthetic prosthesis, however, remains elusive. Although human allograft transplantation and stem-cell engineering seem promising, few patients have been described (most treated on “compassionate” grounds), follow-up is short, and the equipment is expensive and not readily available. Despite impressive advances in tracheal reconstruction, to achieve a laterally rigid, Journal of Reconstructive Microsurgery
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longitudinally flexible, epithelialized, well-integrated, nonimmunogenic, reliable, and durable reconstruction for longsegment tracheal defects continues to be challenging.
25 Ohlsén L, Nordin U. Tracheal reconstruction with perichondrial
grafts. Scand J Plast Reconstr Surg 1976;10(2):135–145 26 Azorin JF, Bertin F, Martinod E, Laskar M. Tracheal replacement
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