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Ann Thorac Surg 1999;68:1043-1051
© 1999 The Society of Thoracic Surgeons
a Division of Thoracic and Cardiovascular Surgery, All Children’s Hospital/University of South Florida School of Medicine, St. Petersburg, Florida, USA
b Division of Otolaryngology, All Children’s Hospital, University of South Florida School of Medicine, St. Petersburg, Florida, USA
c Division of Cardiovascular Surgery, Miami Children’s Hospital, Miami, Florida, USA
d Division of Otolaryngology, Miami Children’s Hospital, Miami, Florida, USA
e Division of Cardiovascular Surgery, University of Iowa, Iowa, USA
f Department of Otolaryngology, University of Iowa, Iowa City, Iowa, USA
g Cardiothoracic Unit, Great Ormond Street Hospital for Children, London, England, UK
h Division of Otolaryngology, University of Bonn, Bonn, Germany
Address reprint requests to Dr Jacobs, Division of Thoracic and Cardiovascular Surgery, All Children’s Hospital, 603 Seventh St S, Suite 450, St. Petersburg, FL 33701
e-mail: jjacobs1{at}compuserve.com
Presented at the Forty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 12–14, 1998.
Abstract
Background. We reviewed both the North American and the total worldwide pediatric experience with tracheal allograft reconstruction as treatment for patients with long segment and recurrent tracheal stenosis.
Methods. The stenosed tracheal segment is opened to widely patent segments. The anterior cartilage is resected and the posterior trachealis muscle or tracheal wall remains. A temporary silastic intraluminal stent is placed and absorbable sutures secure the chemically preserved cadaveric trachea. After initial success with this technique in Europe, several North American centers have now performed the procedure. The cumulative North American experience includes 6 patients (3 adults and 3 children). Worldwide, more than 100 adults and 31 children, aged 5 months to 18 years, with severe long segment tracheal stenosis have undergone tracheal allograft reconstruction.
Results. In North America, 5 of 6 patients have survived, with one early death due to bleeding from a tracheal-innominate artery fistula in a previously irradiated neck. Worldwide, 26 children survived (26 of 31 = 84%) with follow-up from 5 months to 14 years. Only 1 of 26 pediatric survivors (1 of 26 = 3.8%) had a tracheostomy.
Conclusions. Tracheal allograft reconstruction demonstrates encouraging short- to medium-term results for patients with complex tracheal stenosis. Allograft luminal epithelialization supports the expectation of good long-term results.
The diagnosis of tracheal stenosis encompasses a broad spectrum of lesions with varying severity [1, 2]. Long segment tracheal stenosis and recurrent tracheal stenosis can be life-threatening problems [3]. Although resection and primary end-to-end anastomosis has been the initial treatment of choice for most shorter stenoses, this treatment is considered difficult in long segment tracheal stenosis [4]. Numerous other treatment options have been proposed for long segment tracheal stenosis [4–18], but none has been uniformly successful.
Recurrent tracheal stenosis is a particularly challenging surgical problem due to scarring, impaired healing, infection, devascularization, and life-threatening anastomotic disruptions [19]. Like long segment tracheal stenosis, recurrent tracheal stenosis may be treated with a variety of both nonsurgical and surgical options, each with different success rates in different subgroups of patients [19, 20].
Tracheal allograft reconstruction using a cadaveric human tracheal allograft represents a novel therapeutic option for patients with long segment tracheal stenosis, recurrent tracheal stenosis, or both. Tracheal allograft reconstruction was introduced initially by one of us (C.H.) in 1979 as a treatment for tracheal stenosis in adults [21–23]. We then described the application of tracheal allograft reconstruction to more distal tracheal and proximal bronchial lesions in children through the use of median sternotomy and cardiopulmonary bypass [24]. In 1996 we presented our total pediatric experience with 24 children undergoing tracheal allograft reconstruction as the treatment for long segment tracheal stenosis, recurrent tracheal stenosis, or both; this manuscript represented cumulative follow-up of 75.75 patient-years after tracheal allograft reconstruction [25].
After initial success with this technique in Europe, several centers in North America have now performed the procedure. We now report the total North American experience with tracheal allograft reconstruction in 6 patients (3 adults and 3 children) and update the total worldwide pediatric experience that now includes 31 children (with cumulative follow-up of 131.86 patient-years after tracheal allograft reconstruction, or an additional follow-up of 56.11 patient-years since our last publication [25]).
Patients and methods
An international registry and database is maintained for all patients undergoing tracheal allograft reconstruction (CardioAccess Cardiothoracic Surgical Database, CardioAccess Inc, St. Petersburg, FL and Miami, FL). The preoperative, operative, and postoperative courses of all patients of any age undergoing tracheal allograft reconstruction in North America (group A) and all pediatric patients undergoing tracheal allograft reconstruction worldwide (group B) were reviewed.
The North American experience with tracheal allograft reconstruction (group A) included 6 patients: 3 adults and 3 children (tracheal allograft reconstruction performed between September 19, 1996, and February 12, 1998). All 6 patients (aged 2.6–39.4 years, mean ± standard error of the mean [SEM] = 19.8 ± 5.3 years) underwent tracheal allograft reconstruction. All had severe life-threatening recurrent long segment tracheal stenosis and had undergone previous surgical reconstructive attempts. All 6 patients had undergone prior tracheostomy and in addition, these patients had undergone a total of 12 prior tracheal reconstructions (range = 1–4 prior tracheal reconstructions per patient, mean = 2 prior tracheal reconstructions per patient). The prior tracheal reconstructions included 5 rib cartilage tracheoplasties, 3 pericardial patch tracheoplasties, 2 laryngotracheal reconstructions, 1 T-tube tracheoplasty, and 1 resection and primary anastomosis.
In group A, two lesions were congenital long segment tracheal stenoses, two were posttraumatic long segment tracheal stenoses, one was malignant (cystic adenoid carcinoma T1N0M0), and one was inflammatory (relapsing polychondritis). Five patients (83%) required sternotomy and cardiopulmonary bypass for tracheal allograft reconstruction, and 1 patient (17%) underwent tracheal allograft reconstruction via a cervical approach without cardiopulmonary bypass. Further details about these 6 patients in group A are presented in Table 1.
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In group B, 13 lesions were congenital long segment tracheal stenosis, 11 were posttraumatic, and 7 were secondary to prolonged intubation. Twenty-one patients (68%) required neck incisions only. Ten children (32%) required sternotomy. Three patients (10%) without functional airways required stabilization with preoperative ECMO. Further details about these 31 children in group B are presented in Table 2.
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Organ procurement is performed under clean, but not sterile conditions. The trachea is removed circumferentially from the distal end of the larynx to include the first 30 mm of both bronchi. The trachea is then placed in isotonic saline for transport to the allograft bank. Tracheal allograft banks now exist in Miami, Florida, London, England, and Bonn, Germany. (Details regarding these tracheal allograft banks may be obtained from the authors.)
The trachea is stripped of overlying tissue and the trachealis muscle is removed. The remaining anterior cartilaginous portion of the trachea is immersed for a period of 14 days in 500 mL of 4% formalin in compound sodium lactate solution [21–25]. The trachea is then immersed for a period of 56 days in 500 mL of 4 g/L Thimerosal (sodium ethylmercurithiosalicylate, a methiolate related compound) dissolved in Dulbecco phosphate-buffered saline. It is then stored in acetone for a minimum of 10 days before its release for clinical use. The allograft may be used up to 2 years after procurement. All processing and final storage is in autoclavable and acetone-resistant Nalgene polypropylene bottles (Nalgene, Sybron, Rochester, NY). Five samples of the excised trachealis muscle undergo the same processing until the final stage in acetone, at which point they are used for microbiological testing. They are tested for aerobic bacteria, anaerobic bacteria, fungi, mycobacteria, and hypothermic microorganisms.
Before insertion, the allograft is washed thoroughly in saline. Histological studies confirm that all cells in the graft die and all major histocompatibility complex markers are lost [21, 22, 26].
Preoperative work-up
Patients undergo preoperative pulmonary function testing, preoperative radiographic testing (chest radiograph, dynamic computed tomography scan with three-dimensional tracheal reconstruction, tracheal magnetic resonance imaging [Fig 1]), vocal cord evaluation, and bronchoscopy (rigid and flexible).
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Exposure of the trachea via a transverse neck incision is identical to standard approaches. Utilizing a mixture of sharp and blunt dissections, the trachea is exposed beneath the pretracheal fascia. Care is taken to avoid the head vessels, recurrent laryngeal nerves, and the pulmonary artery during dissection.
For the patients undergoing an approach via median sternotomy, the patient is positioned supine, and the skin is prepared and draped to expose the neck and chest. Potential incision sites are marked with a surgical marker pen. A conventional median sternotomy is performed and the thymus excised. Before opening the pericardium, the head vessels are dissected and vascular slings passed around them to permit retraction. The pretracheal fascia is opened in the midline and the upper trachea identified. The upper tracheal lumen may be difficult to identify in situations in which the patient has complete separation of the upper airway from the lower airway with the upper airway ending in a blind pouch (a common situation in this subgroup of patients). Simultaneous dissection and bronchoscopy may be helpful.
The pericardium is then opened longitudinally and stay sutures applied. The superior caval vein, the aorta, the pulmonary arteries, and the innominate vein are mobilized and vascular slings or tapes passed around them to facilitate retraction. Heparin is given and purse strings inserted into the upper left aspect of the aorta and the right atrial appendage. A flexible, wire-wound aortic cannula is preferred to permit safe and repeated repositioning. A right-angled venous cannula or a dual stage venous cannula is used for venous drainage. The bypass is run at a temperature between 32°C and 37°C, and with a hematocrit > 35%.
The trachea is exposed further between the aorta and the superior caval vein. The incision in the pretracheal fascia is continued down to below the lower limit of the stenosis. Both the left and right main stem bronchi can be exposed and mobilized if necessary. With these maneuvers, it is often possible to treat very long segment stenoses, often extending from cricoid cartilage superiorly to below the carina inferiorly.
Once safely established on cardiopulmonary bypass, the anterior trachea is incised longitudinally in the middle of the stenosis. At this stage one must make a decision as to the preferred procedure, because it is still possible to perform a slide tracheoplasty, augmentation tracheoplasty with rib cartilage or pericardium, or other conservative operation if preferred. Once the surgeon has decided to perform tracheal allograft reconstruction, the anterior incision in the trachea is continued both cephalad and caudad until normal trachea or bronchus is reached. The lateral walls of the narrowed segment may then be removed, leaving only the posterior wall in continuity. During this dissection, the recurrent laryngeal nerves are avoided by keeping within the trachea.
It is often necessary to create a series of longitudinal, partial thickness slits in the posterior remnant in patients with complete tracheal rings or rigid scar tissue down the posterior wall of the trachea. On cardiopulmonary bypass, electrocautery is the preferred method for creating these incisions to minimize hemorrhage. The rationale for these slit incisions is to create partially everted margins in the posterior wall in settings in which that component is made of solid cartilage or complete tracheal rings. The everted margins reflect a splayed-out posterior wall creating an advantageous morphology to receive the tracheal allograft.
One or two temporary silicone intraluminal stents (Dumon stents, Axiom, Lyon, France or Hood "Bronchial stent with posts," Hood Laboratories, Pembroke, MA) then may be placed onto the posterior wall and sutured to the native trachea with 4 to 6 single absorbable monofilament sutures. These sutures are placed at the upper and lower ends of the stents to minimize movement of the stents. The stent(s) will support the tracheal allograft, which undergoes an initial period of softening in the early days after insertion. (Alternatively, a temporary tracheostomy tube may be used to stent the allograft as was done in 1 small child in this series.)
Before proceeding to the next stage, the endotracheal tube can be repositioned under direct vision to lie inside the upper orifice of the Dumon/Hood stent. The graft is then trimmed to reflect the defect in the anterior and lateral trachea before being sutured in place with horizontal-mattress, absorbable monofilament sutures. We prefer polydioxanone suture (PDS) material rather than polyglactin 910 (Vicryl) suture material (Ethicon, Inc, Somerville, NJ) [34]. These horizontal mattress sutures join the allograft to the posterior tracheal remnant.
Intraoperative bronchoscopy is performed to confirm graft patency and to allow bronchial toilet. The suture line of the allograft anastomosis may be sealed and made air tight with Tisseel fibrin glue (Immuno AG, Vienna, Austria). Cardiopulmonary bypass, if utilized, is weaned. Hemostasis and routine closure follow.
Postoperative care
All patients require intensive care unit support and benefit from a multidisciplinary approach involving cardiac surgeons, intensivists, otolaryngologists, and especially dedicated nurses and respiratory therapists. Emergency skilled bronchoscopy must be readily available for treatment of acute airway problems. Frequent postoperative rigid bronchoscopy may be necessary to clear granulation tissue for several weeks as the allograft undergoes epithelization, especially in smaller patients. Local temporary stenoses from exuberant granulation tissue may be treated with balloon dilatation through the rigid bronchoscope. Granulation tissue also may be removed with bronchoscopic cup biopsy forceps or electrocautery. Laser is avoided as long as the silastic endotracheal stents are in place. Postoperative antibiotic coverage is tailored to the preoperative and intraoperative sputum cultures. Pseudomonas is covered with two intravenous antibiotics that act by different mechanisms as well as by inhalational coverage. Inhaled and occasionally intravenous steroids are utilized to help decrease granulation tissue. Adrenaline nebulizers also are used.
The intraluminal stent supports the allograft until the allograft hardens and reepithelialization has occurred. After bronchoscopy visually confirms that granulation tissue no longer exists and that the inner surface of the allograft has undergone reepithelialization, the stent is removed. Endoscopic stent removal is usually not difficult because the absorbable sutures previously holding the stent will have dissolved. The stent can be grasped, rotated medially, folded onto itself, and withdrawn. After discharge from the hospital, bronchoscopic follow up is utilized. Immunosuppression is not utilized.
Results
In group A, early mortality occurred in 1 patient (1 of 6 = 17%) who underwent tracheal allograft reconstruction after a previous curative resection and primary anastomosis for cystic adenoid carcinoma (T1N0M0), which was followed by 6000 rads of cervical radiation at another institution and subsequent anastomotic disruption requiring creation of a "permanent" mediastinal tracheostomy. This mediastinal tracheostomy was painful and unstable; thus, the patient was referred for tracheal allograft reconstruction. Because of concern about the prior high dose cervical radiation, a pectoral muscle flap was rotated into the neck to vascularize the reconstruction and seal the tracheal allograft reconstruction. The patient was extubated on the morning of postoperative day 1 and was able to speak for the first time in 10 months. Although he initially did well, his muscle flap required revision and on postoperative day 12, he sustained a lethal hemorrhage from a tracheal-innominate artery fistula.
Late mortality in group A is zero. Follow-up has ranged from 0.57 to 2.44 years (mean ± SEM = 1.68 ± 0.39 years). Of the 5 survivors (5 of 6 = 83%), 2 patients still have their stents in place. (One of these patients had allograft placed from the cricoid to the carina and the other had allograft over approximately 
of the trachea.) Both had their stents removed, developed tracheomalacia at the allograft site, and requested stent replacement due to difficulty breathing on exertion. Both are living active lives with the stents in place.
A third child, with allograft placed from the cricoid to the carina to reconstruct a severely unstable airway with a mediastinal tracheostomy, had his stents removed, replaced due to tracheomalacia, and recently removed again; he is currently stent free and requires occasional bronchoscopic removal of granulation tissue within the airway. The fourth patient had a temporary tracheostomy after tracheal allograft reconstruction but is now decanulated, without stents, and with a stable airway. Finally, 1 small child still has a tracheostomy stenting the allograft.
The 5 survivors have all demonstrated functional tracheal allografts, with bronchoscopy revealing reepithelialization of the lumen. Previously published histologic studies have confirmed the presence of ciliated respiratory epithelium coating the lumen of the allograft [25]. We have documented the migration of this epithelium from the posterior tracheal remnant to the lateral and eventually the anterior allograft walls (Fig 2). No patient has demonstrated rejection or required immunosuppression. No patient has demonstrated allograft calcification either clinically or radiographically. Objective pulmonary function testing has documented dramatic improvement after tracheal allograft reconstruction (Fig 3). No patient has developed new onset of vocal cord paralysis after tracheal allograft reconstruction.
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Late mortality occurred in four patients (4 of 31 = 12.9%); however, only 2 patients (2 of 31 = 6.4%) died late with tracheal problems. One infant with congenital long segment tracheal stenosis had a sepsis-related anastomotic dehiscence after primary tracheoplasty and then a failed patch revision. Subsequent mediastinitis required ECMO support. This infant later underwent tracheal allograft reconstruction after 4 days of ECMO to allow for local control of sepsis. The airway stabilized sufficiently to allow separation from ECMO 3 days after tracheal allograft reconstruction, but the child died 3.5 months later secondary to further sepsis and airway failure. A second small child died 4 months after tracheal allograft reconstruction from acute hemorrhage thought to be due to granulation tissue or pulmonary hemorrhage.
Two other patients died late with functional airways. One victim of multiple trauma died from cardiac failure despite a completely functional airway after tracheal allograft reconstruction. A second late death occurred in a child with recurrent congenital long segment tracheal stenosis who died 18 months after tracheal allograft reconstruction from unrelated gastrointestinal problems despite a completely functional airway.
Twenty-six patients survive (26 of 31 = 84%). Follow-up has ranged from 5 months to 14 years (mean ± SEM = 5.07 ± 0.78 years). Twenty-two patients are now asymptomatic and without airway problems. These 22 children have all demonstrated stable and functional tracheal allografts, with bronchoscopy revealing reepithelialization of the lumen. Four children are still undergoing treatment. Of these, 1 patient has a tracheostomy tube stenting the allograft and 1 has intraluminal stents in place supporting the allograft as described above.
Similar to group A, no patient has demonstrated rejection or required immunosuppression and no patient has demonstrated allograft calcification either clinically or radiographically.
Only 1 patient survives of the 3 patients who required preoperative ECMO [35]. At another institution, this 5-month-old infant failed attempted balloon dilation for congenital long segment tracheal stenosis and sustained a cardiopulmonary arrest after the procedure requiring the initiation of ECMO. Four days later, tracheal allograft reconstruction was performed and ECMO was discontinued. The child was at home, without major airway problems, and growing normally [35]. However, tracheal stenosis recurred and was treated with a second tracheal allograft reconstruction 14.5 months after the original replacement.
Comment
Tracheal allograft reconstruction represents a therapeutic modality with encouraging short- to medium-term results for patients with complex recurrent long segment tracheal stenosis who have not responded to conventional management. Numerous techniques have been described for the treatment of long segment tracheal stenosis and recurrent tracheal stenosis, including endobronchial stenting [20], aggressive balloon dilation [9, 10], pericardial patch tracheoplasty [11–13], cartilage and rib graft tracheoplasty [14–16], omental pedicle flap tracheobronchial reconstruction [17], slide tracheoplasty [6, 8], and recently, the tracheal autograft [18]. Nevertheless, an important subgroup of patients exists who do not respond to these conventional treatments. Tracheal allograft reconstruction allows tracheal reconstruction when less of the patient’s own tracheal tissue is available and allows tracheal reconstruction when conventional treatment may be considered impossible or dangerous.
Tracheal allografts have been studied extensively in the laboratory setting. Tracheal allografts not subjected to chemical preparation and transplanted in animal models are subject to immunological recognition and rejection [36, 37]. Allogenic vascularized transplants with the use of immunosuppression have been studied in dogs, but have not been applied successfully to humans [38].
Methiolate-preserved cartilage has also been investigated in the laboratory [39]. The methiolate-preserved allograft has the characteristics of both avascularity and avitality [21, 26, 39]. The chemical preparation has been shown to destroy the allograft’s immunological antigens [40]. Thus, immunosuppression is thought not necessary. The chemically treated and preserved allograft acts as a biocompatable implant with no intrinsic cellular viability. It can be thought of as a skeleton, allowing fibroblasts to grow inward between cartilage rings and eventually permitting epithelialization from within the lumen. Immunological investigation in humans has demonstrated the absence of evidence of systemic immunoactivation or signs of clinical rejection after tracheal allograft reconstruction [26].
The success with tracheal allograft reconstruction in adults [21–23] led to the eventual pediatric application of this technique [24, 25]. All but 2 of the pediatric cases of tracheal allograft reconstruction were in the setting of previous tracheal reconstructive attempts. Many of these had failed several conventional tracheal reconstructive procedures such as balloon dilatation, tracheal resection and reanastomosis, pericardial patch tracheoplasty, and rib cartilage tracheoplasty at a variety of institutions. All were thought to be poor candidates for further standard conventional procedures because of the severity of their tracheal disease, the degree of tracheal thickening, and the large amount of scar tissue secondary to previous interventions. Previous tracheal procedures often resulted in poor tracheal blood supply and decreased tracheal mobility. Because of this lack of mobility and compromised tracheal blood supply, tracheal allograft reconstruction was used. The success of tracheal allograft reconstruction in Europe in patients with recurrent stenosis after conventional tracheal reconstructive techniques made tracheal allograft reconstruction an appealing option. Consequently the application of tracheal allograft reconstruction has extended to North America.
The tracheal allograft has numerous advantages including adequate availability, nearly circumferential tissue for reconstruction, and a carina that may be used to permit extensive repair. In addition, the procedure can be repeated if required. Follow-up bronchoscopic and histologic studies have shown clear evidence of luminal epithelialization. Ciliated columnar respiratory epithelium has been shown to cover the lumen of the allograft [21–27].
An important possible disadvantage of tracheal allograft reconstruction in children is that the growth potential of the tracheal allograft is not known. Although the remaining autogenous trachea may grow, no evidence exists to suggest that the tracheal allograft itself will grow. However, by using an oversized allograft in children, problems related to lack of allograft growth have been avoided. Of course, tracheal allograft reconstruction can be repeated if necessary.
A second disadvantage of tracheal allograft reconstruction is the apparent necessity of long-term tracheal stenting when longer segments of trachea with greater circumference are replaced with allograft. This tracheomalacia of the allograft may be prevented by modifying the chemical preservation (possibly by replacing the formaldehyde with gluteraldehyde or eliminating the acetone, or both) or even by using cryopreserved tracheas. We are investigating these ideas in the laboratory, as are other investigators.
The role of tracheal allograft reconstruction in the management of tracheal disease is not yet established. Tracheal allograft reconstruction certainly represents an important additional option for the treatment of severe long segment tracheal stenosis or recurrent tracheal stenosis. Primary short segment stenosis is still best treated with resection and end-to-end anastomosis. For primary long segment tracheal stenosis, if nonoperative treatment fails, slide tracheoplasty, pericardial patch tracheoplasty, and rib cartilage tracheoplasty and tracheal autograft reconstruction are all reasonable treatment options. For recurrent long segment tracheal stenosis, the best treatment remains unclear and treatment strategies continue to evolve. Tracheal allograft reconstruction offers an effective alternative in this setting, especially when patients have failed more conventional treatment modalities. Tracheal allograft reconstruction should be seen currently as an addition to the available list of therapeutic options for tracheal stenosis, not as a replacement for them.
To establish further the role of tracheal allograft reconstruction in the management of tracheal disease, we are maintaining an international registry and database of all patients undergoing tracheal allograft reconstruction (a component of the CardioAccess Cardiothoracic Surgical Database, CardioAccess Inc, St. Petersburg, FL and Miami, FL). Studies are now underway to evaluate long-term airway and pulmonary function.
Tracheal allograft reconstruction demonstrates encouraging short- to medium-term results for patients with complex tracheal stenosis. Postoperative bronchoscopic and histologic studies provide evidence of epithelialization and support the expectation of good long-term results.
Acknowledgments
Richard A. Jonas, MD, Cardiovascular Surgeon-in-Chief, Boston Children’s Hospital, Harvard Medical School, contributed a patient to this series, and reviewed and commented on the manuscript.
Footnotes
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/
References
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