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Right arrow Trachea and bronchi

Ann Thorac Surg 2006;81:1068-1074
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Carinal Replacement With an Aortic Allograft

Agathe Seguin, MD a , b , * , Emmanuel Martinod, MD, PhD a , b , Marianne Kambouchner, MD c , Gabriella O. Campo, MD a , Pascale Dhote, MD a , Patrick Bruneval, MD d , Jacques F. Azorin, MD b , Alain Carpentier, MD, PhD a

a Laboratoire d'Etude des Greffes et Prothèses Cardiaques, Hôpital Broussais, Paris, France
b Service de Chirurgie Thoracique et Vasculaire, Hôpital Avicenne, Paris, France
c Service d'Anatomo-Pathologie, Hôpital Avicenne, Paris, France
d Service d'Anatomo-Pathologie, Hôpital Européen George Pompidou, Paris, France

Accepted for publication July 25, 2005.

* Address correspondence to Dr Seguin, Laboratoire d'Etude des Greffes et Prothèses Cardiaques, Hôpital Broussais, Pavillon René Leriche, 96, rue Didot, Paris, 75674 Cedex 14 France (Email: agatheseguin{at}wanadoo.fr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Carinal replacement after extensive resection remains a tremendous challenge in thoracic surgery. In previous studies, we demonstrated that an aortic graft could be a valuable tracheal substitute. The goal of this new study was to evaluate the reconstruction of the carina using a stent supported bifurcated aortic allograft.

METHODS: In 15 sheep the replacement of the tracheobronchial bifurcation with an aortic allograft was performed under cardiopulmonary bypass. A temporary stent prevented airway collapse. No immunosuppression was used. Aortic segments were retrieved at regular intervals up to 24 months after implantation.

RESULTS: All animals survived the initial aortic allograft operation. Six animals died postoperatively (1 of graft necrosis, 2 of pneumonia, and 3 of bronchial fistula). The remaining 9 animals were in good condition until they were euthanized. Stent removal was tolerated after 9 months in 3 animals. Progressive transformation of the arterial graft initially into extensive inflammatory tissue, and after 3 to 6 months into a tracheal tissue comprising a well-differentiated epithelium and cartilage was confirmed by histology.

CONCLUSIONS: This study showed that regeneration of a functional tissue can be obtained after replacement of the carina with an aortic allograft. The origin and mechanisms of this regenerative process remains to be discovered. These results represent an important hope for the reconstruction of the carina after extensive resection, especially for cancer lesions. In human application, the systemic use of omentoplasty or myoplasty should further reduce its risk of complication.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The reconstruction of the carina after extensive resection remains a tremendous challenge and one of the most technically demanding of all thoracic procedures. Extensive tracheocarinal resection is required not only in patients with malignancies involving the carina or the trachea, but also in patients with benign stenosis of the airway secondary to traumatic, congenital, inflammatory, or iatrogenic lesions [1]. Numerous techniques have been described to date to confront the challenge of carinal reconstruction. In 1957, Barclay and colleagues [2] reported the first human case of carinal reconstruction after resection.

Patients with major anatomical defects after resection of a carinal lesion are at risk of postoperative complications such as ischemia, stenosis, and disruption of the anastomosis resulting from excess tension. The length of the airway that can be resected varies from patient to patient regarding several criteria such as age, body habitus, prior operations, and disease process. Mathisen [3] reported that carinal lesions more than 4 cm in length should not be proposed for resection because of the risk of excessive postoperative tension. Extensive tracheocarinal defects may require the use of a graft. Autogenous tissues and artificial prostheses have not proved clinically useful for carinal reconstruction [4–7]. Several experimental studies on carinal transplantation have been performed with promising results [8, 9]. However the need of immunosuppressive treatment is a serious limitation.

In previous studies we demonstrated that an aortic graft (autologous or homologous) could be a valuable tracheal substitute [10, 11]. This conduit was selected because of specific advantages such as similar diameter, elasticity, and resistance to infection. In this study, we evaluated the replacement of the carina with a fresh aortic allograft in sheep.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Allograft Preparation
In 15 female sheep (weight, 30 to 35 kg), the ascending aorta, the descending aorta, and the common brachiocephalic artery were harvested to provide a bifurcated aortic allograft (Fig 1). Two blood units were also harvested for the priming of the cardiopulmonary bypass during the procedure.


Figure 1
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  		Fig 1. Sheep aortic allograft: (a) anatomic figure and (b) harvested allograft. (1 = anterior [ascending] aorta; 2 = posterior [descending] aorta; 3 = common brachiocephalic artery).

 
The aortic allograft was preserved with a solution used in human practice (Table 1). The mean duration of preservation was 4 days (range, 1 to 17 days) as recommended by others [12].


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  		Table 1. Solution of Preservation for the Aortic Allograft
 
Experimental Design
Fifteen female sheep weighing 28 to 41 kg were used. The mean age of the animals was 8 months. All animals received care in compliance with the Guide for the Care and Use of Laboratory Animals prepared by the Institute of Laboratory Animal Resources, National Research Councils, and published by the National Academy Press, revised 1996.

Anesthesia
After induction with intravenous propofol (1%; 6 mg/kg) and endotracheal intubation, ventilation was performed with a Siemens 900 C ventilator (Siemens, Solna, Sweden) (tidal volume 10 mL/kg, 24 breaths/min). Anesthesia was maintained with inhaled 60% oxygen and 1% to 2% isoflurane until the carinal resection. Oxygenation was then carried out by an extracorporeal circulation, and anesthesia was maintained intravenously by propofol (40 mL/h) and ketamine (5 mL/h).

Continuous arterial blood pressure and pulse oximetry were intraoperatively monitored. All animals were perfused with a crystalloid solution (10 mg/kG/h) and with 1 blood unit if necessary. Once awake, animals were immediately extubated. One gram of cefazolin was injected for 8 days after the operation.

Surgical Procedure
After a right thoracotomy in the fourth intercostal space, the tracheal bifurcation was dissected. A cardiopulmonary bypass was carried out to maintain the hematosis between the right atrium and the descending aorta after general anticoagulation with heparin (0.5 mg/kg). The carina was resected (trachea = 3 cm; mainstem bronchi = 1 cm) and the aortic allograft was interposed. The limits of the aortic graft were marked with a biological ink used in aesthetic surgery. First the left and right anastomoses of the mainstem bronchus were performed and then the posterior wall of the proximal tracheal anastomosis (Fig 2). A removable bifurcated Endoxane stent (Novatech, La Ciotat, France) was placed in the lumen of the aortic graft under direct vision, which was then controlled by fiberscopy. The tracheal anastomosis was anteriorly completed and the extracorporeal circulation was discontinued. Two thoracostomy tubes were left in place for 6 hours.


Figure 2
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  		Fig 2. Operative view of the carinal resection and reconstruction with the aortic allograft.

 
Clinical Evaluation
Post-procedure monitoring was performed daily for 1 week, followed by monthly examinations to assess weight, respiratory, and overall condition of the animals. This evaluation included a fiberscopic examination (BPF Storz; Karl Storz Endoscopie, France) under sedation (propofol) at 1, 3, 6, 9, 12, and 18 months to assess the viability of the aortic allograft. Chest roentgenograms were performed at 1, 3, 6, 9, 12, 18, and 24 months to detect a stent migration and pulmonary complications.

Histologic Evaluation
Animals were euthanized at 1, 3, 6, 9, 12, 18, and 24 months with an intravenous injection of potassium chloride and propofol to explant the grafts. En bloc resection of the heart and lung organs with surrounding tissues was performed and subjected to macroscopic and microscopic examinations. After removal of the bifurcated stent and macroscopic evaluation of the graft, postmortem specimens were immediately placed in a 10% formaldehyde solution. Specimens were embedded in paraffin, and 3-µm sections were stained with hematoxylin eosin staining and orcein for light microscopy. Special attention was directed toward microscopic evidence of inflammation, morphologic transformation of the graft, and ink marker of the anastomotic lineage.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Results are presented in Table 2. All animals survived the operation.


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  		Table 2. Complications, Follow-Up, Fiberscopic, and Histologic Examinations
 
In the early postoperative period, all animals experienced an irritating cough with no dyspnea or effort limitation.

One animal died postoperatively of pneumonia at day 15. Postmortem examination showed an airway collapse in the right segment of the reconstruction, likely due to a stent size insufficiency. One animal died at postoperative day 20. Postmortem examination showed a necrotic graft free of any fistula or infection. Two animals experienced pneumonia at days 18 and 21 postoperatively and were treated successfully with antiobiotic therapy for 1 week. One of them died postoperatively at 6 weeks from extensive pneumonia that was confirmed by autopsy.

At 6 weeks, 2 animals experienced a cataclysmic hemoptysis leading to death. Postmortem examination showed a necrotic graft associated with a fistula between the descending aorta and the left segment of the graft, likely caused by stent erosion. At 5 months, 1 animal died from an empyema. Postmortem examination showed a bronchopleural fistula on its left side.

In the 9 remaining animals, the long-term follow-up showed the absence of complications and an average weight gain of 50%. In all animals, chest roentgenograms confirmed that both lungs were well inflated with no atelectasis. Bronchoscopic evaluations did not reveal anastomotic leakage, graft rupture, stenosis, or granulation in the region of the anastomoses. In all animals, neither stent migration nor retention of sputum in the lumen of the stent was observed. In 3 animals, the stent was easily removed at 9 months under a rigid bronchoscopic procedure and spontaneous ventilation. During this procedure we did not observe airway collapse. After removal, animals did not show any respiratory impairment or stenosis within a 15-month follow-up period.

Carinal specimens removed at different intervals after the operation allowed us to follow the histologic evolution of the engrafted aortic tissue. At 1 month the aortic tissue was replaced by an intensive inflammatory reaction with no epithelium organization. Disorganized elastic fibers were observed within the aortic graft, the numbers of which decreased as the follow-up progressed; few remnants were still present at 24 months (Fig 3). At 3 months, the inflammatory reaction was still important and a nonkeratinizing metaplastic squamous epithelium was observed near the anastomoses. After 3 to 6 months, the repair process was completed with the formation of a continuous epithelium polystratified in the center of the graft and mucociliary near the anastomoses (Fig 4). From 1 to 6 months, no cartilage differentiation was observed in the graft. At 6 months, islands of immature cartilage appeared near the anastomoses, whereas no cartilage regeneration was seen in the center of the graft (Fig 5). In the sheep sacrificed at 24 months in which the stent had been removed at 9 months, continuous mucociliary epithelium and cartilaginous formations were observed (Fig 4, Fig 5).


Figure 3
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  		Fig 3. Histological examination at 3 months showing disorganized elastic fibers (star) from the aortic allograft and new immature cells (arrow). (A) (Hematoxylin and eosin; x250). (B) (Hematoxylin and eosin; x400). (C) At 24 months few elastic fibres are still present within the graft. (Orcein staining; x250.)

 

Figure 4
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  		Fig 4. Histological examination at different stages of follow-up from 1 to 24 months, showing the successive steps of epithelium regeneration from (A) squamous to (B) pseudostratified to (C) mucociliary (Hematoxylin and eosin; x250 and x400).

 

Figure 5
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  		Fig 5. Histological examination showing (A) islands of immature cartilage at 6 months and (B) mature cartilaginous formations at 24 months. (Hematoxylin and eosin; x400 and x250.)

 
Ink markers placed at the site of anastomoses were not found in the graft in spite of their biological compatibility and durability. A significant contraction representing 50% of the total graft length was observed in all specimens. However, the morphology of the bifurcation was preserved (Fig 6).


Figure 6
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  		Fig 6. Macroscopic view of a neocarina after 12 months. The suture lines (arrows) delineate the regenerated tracheal bifurcation.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Extensive tracheocarinal resection is required in patients with malignancies involving the carina and the trachea, or in patients with benign stenosis of the airway secondary to traumatic, congenital, inflammatory, or iatrogenic lesions. Carinal reconstruction is one of the most difficult operations in general thoracic surgery, with high morbidity and mortality rates [3]. Airway resection and reconstruction provide the most reliable definitive correction. Many procedures of reconstruction have been reported [13]. The method described by Barclay and colleagues remains the standard for the reconstruction of the carina [2]. This allows the anastomosis of the trachea to the right main bronchus after the division of the pulmonary ligament and then the end-to-side anastomosis of the left main bronchus to the bronchus intermediary. Primary reconstruction requires a tracheobronchial gap less than 6 cm in length. However, many patients are not suitable for surgery because of the extent of the disease. For these patients a palliative method (ie, airway stenting under bronchoscopy) is performed [14].

Although tracheoplasty has been described in carinal reconstruction using a patch of autologous tissues, such as the pericardium [5], cartilage or rib [4], or nonviable chemically preserved tracheal graft [15], these techniques are not feasible in patients with circumferential involvement of the tracheobronchial bifurcation. Carinal replacement or transplantation has been proposed as useful techniques for the management of critical carinal lesions. Experimental trials in carinal replacement are limited and their conclusions are similar to those reported in tracheal replacement. Prosthetic materials have been used for carinal reconstruction, but yield limited success due to chronic infection, migration, erosion of major blood vessels, and proliferation of granulation tissue [6, 7, 16]. Several studies have been performed in order to evaluate the carinal allograft transplantation. As for tracheal transplantation, carinal transplantation has not provided sufficient results to consider a clinical application regarding the graft ischemia that led to necrosis and stenosis [8]. The tracheal graft became ischemic, which was likely due to excessive devascularization. In fact, the carina has a poor blood supply from the bronchial and oesophageal arteries, and moreover, there are no organs adjacent to the carina that can supply a good blood flow to the graft. Revascularization of the graft was insufficient, despite the use of an omentoplasty [9]. In addition, immunosuppressive therapy is mandatory because tracheal allografts transplanted in animal models are subject to immunological recognition and rejection. Although graft cryopreservation allows long preservation and reduces antigenicity [17–19], chronic rejection responses persist that often result in progressive graft atrophy [20]. Numerous problems remain to be solved with carinal allografts. Efforts must be made to define techniques of graft preservation, to maintain the blood supply to the graft, and to minimize the effect of a concomitant immunosuppressive treatment [8].

In a previous work, we showed that a living autologous aortic segment could be a valuable substitute to the trachea for periods as great as 3 years. The aortic graft was progressively replaced by a tracheal structure comprising mucociliary epithelium and newly formed cartilage [10]. In a second work we demonstrated that fresh aortic allograft led to similar results [11]. In potential clinical applications, aortic allograft from donor patients represents a better option that would avoid the need to harvest the aorta from the intended tracheal recipient patient. As suggested by major clinical studies in vascular surgery, immunosuppressive treatment is not required with aortic allograft, thus this technique can be used in malignant diseases [12].

The present study demonstrated that replacement of the carina with an aortic allograft could remain functional for periods of as many as 24 months. The well-known, difficult surgical conditions of carinal replacement in a sheep model may explain the mortality rate of 40% in this preliminary experimental evaluation. Two animals presented a left bronchovascular fistula secondary to stent erosion of the graft, a complication caused by the closer proximity of the aorta to the left mainstem bronchus in sheep than in humans. This complication could be minimized in humans by the systematic use of omental or muscle flaps. Several studies have shown that omentum or muscle flaps are effective at promoting revascularization [21, 22]. In addition, early removal of the stent may also minimize the risk of vessel erosion facilitated by the rigidity of the prosthesis. However, the removal of the stent must not take place before 6 months as shown by our previous experiments [11]. Carinal replacement may require a longer period of stenting, for as much as 9 months, as suggested by our first histologic examinations. In all animals, removal of the stent was well tolerated.

As observed in tracheal replacement, histologic findings are the most intriguing aspects of this study. The regeneration of the epithelium from the native trachea has been well documented in our previous works and in other studies. The epithelial regeneration represents a critical point in carinal and tracheal reconstruction to provide a durable solution. Islands of chondrocytes were observed in the graft at 6 and 9 months near the anastomotic lineages. This marks the first time that experimental carinal replacement shows the possibility of a progressive transformation of the graft into a tracheal structure comprising respiratory epithelium and chondrocytes. Cartilage formation is necessary to avoid airway collapse at the time of stent removal. Tissue transformation can be obtained at the molecular level by physical factors such as electrical or mechanical stress [23, 24]. In this study the regenerative process was slower than observed after tracheal replacement with an aortic graft. This can be explained by the characteristics of the carinal region that is well known for its poor vascularization and reduced mechanical constraints. A significant longitudinal contraction was observed between the tracheal anastomosis and the bronchial anastomosis representing as much as 50% of the total graft length; however the normal morphology of the bifurcation was preserved with new cartilaginous formations playing a major role. There was no native old cartilage in the area of bifurcation, and there was not any stenosis of the anastomoses. Unfortunately, ink markers left on native cartilaginous rings during the operation were not found by histologic examination. Further experiments using fine steel wire in order to permanently mark native cartilaginous rings at proximal and distal anastomoses are in progress.

In previous experiments using a polymerase chain reaction technique and chromosome-Y identification in female sheep having received a male aorta, we demonstrated that the regenerated cartilage derived from the recipient (most probably from mesenchymatous cells or bone marrow cells) were triggered by local signals of differentiation at the site of engraftment [11]. The role of stem cells and progenitor cells has been shown in regeneration of destructed areas of tissues or organs such as the heart, liver, brain, kidneys, vessels, or tracheal cartilage [25–32]. A sex mismatched combination already investigated in a previous study was not found to be necessary in this study. The important question of the mechanism of cartilage regeneration requires further studies.

These results offer new perspectives in human carinal reconstruction. The use of a fresh aortic allograft could be preferable to the use of a cryopreserved aorta due to higher cell viability in the former. Radiologic studies in humans indicate that carina and iliac bifurcation have similar diameters, suggesting that iliac bifurcation could be a suitable graft for carinal replacement in the future. Only two studies in which an aortic allograft are been used to replace the trachea have been published, but neither report the formation of cartilage [33, 34]. Our methods were more successful than these groups, perhaps due to a shorter follow-up time (14 days) [34], as well as a prosthesis technique used to protect the aorta from inflammatory response [33]. Only one clinical study reports the use of a fresh autologous artery tissue as patch plasty for long-segment congenital tracheal stenosis with success [35].

This study confirms that an aortic allograft is a valuable substitute for carinal replacement and represents an important hope for the reconstruction of the carina after an extensive resection, especially for patients with malignant lesions who are still treated by palliative methods. In such patients, this technique seems to be crucial as no immunosuppressive treatment is necessary. In human application, the use of omentoplasty or myoplasty should be implemented to improve not only the vascularization but also the protection of the aortic graft and thus to avoid the lethal complications observed in our study. The origin of the regenerative process remains to be discovered and new experimental trials are underway to elucidate the histologic transformation of aortic tissue into a tracheal structure.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was supported by a grant from the University Pierre and Marie Curie of Paris, the Foundation for the Medical Research and by The Alain Carpentier Foundation. We thank Nathalie Goussef, Martine Rancic, Amélie Pires-Alves, Marie Samsoen, and Cyril Schneider-Maunoury for their technical assistance. We also thank Thomas Matthiesen for helpful advice and critical review of this article. The bifurcated Endoxane stents were kindly provided by the Novatech Laboratory, La Ciotat, France).


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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Agathe Seguin
Emmanuel Martinod
Jacques F. Azorin
Alain Carpentier
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