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Right arrow Trachea and bronchi

Ann Thorac Surg 2003;75:1572-1578
© 2003 The Society of Thoracic Surgeons

Original article: general thoracic

Long-term evaluation of the replacement of the trachea with an autologous aortic graft

Emmanuel Martinod, MDa,b*, Agathe Seguin, MDa, Karel Pfeuty, MDa, Paul Fornes, MDa, Marianne Kambouchner, MDb, Jacques F. Azorin, MDb, Alain F. Carpentier, MD, PhDa

a Laboratoire d’Etude des Greffes et Prothèses Cardiaques, Hôpital Broussais, Upres 264, Université Paris 6, France
b Department of Thoracic and Vascular Surgery, Hôpital Avicenne, Assistance Publique-Hôpitaux de Paris and UFR SMBH, Bobigny, Université Paris 13, France

Accepted for publication January 7, 2003.

* Address reprint requests to Dr Martinod, Service de Chirurgie Thoracique et Vasculaire, Hôpital Avicenne, 125 route de Stalingrad, 93000 Bobigny, France.
e-mail: emartinod{at}wanadoo.fr


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: Tracheal reconstruction after extensive resection remains a challenge in thoracic surgery. The goal of this experimental study was to analyze the long-term evolution of tracheal replacement using an autologous aortic graft.

METHODS: In 21 sheep, a 5-cm segment of the cervical trachea was replaced by a segment of the descending thoracic aorta that was reconstructed to a prosthetic graft. Because of the airway collapse reported in a previous series, a permanent (n = 13) or temporary (n = 8) stent was systematically placed in the lumen of the graft. Clinical, bronchoscopic, and histologic examinations were performed up to 3 years after implantation.

RESULTS: All animals survived the operation with no paraplegia. In the group with a permanent stent, three complications occurred: one stent displacement, one laryngeal edema, and one infection. Stent removal was tolerated after 6 months in the group with a temporary stent. Histologic examination showed a progressive transformation of the arterial segment into first extensive inflammatory tissue with a squamous epithelium, and after 6 to 36 months well-differentiated tracheal tissue including a continuous mucociliary epithelium and regular rings of newly formed cartilage.

CONCLUSIONS: An autologous aortic graft used as a substitute for extensive tracheal replacement in sheep remained functional for periods up to 3 years. The progressive transformation of the graft into a structure resembling tracheal tissue seems to be a key factor in long-term patency. The mechanism of this regenerative process and the possibility of using arterial homografts, which would make clinical application easier, remain to be evaluated.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Tracheal reconstruction after extensive resection remains a challenge in thoracic surgery. Many investigators have attempted to find the ideal tracheal substitute using prosthetic or biologic materials, including various autologous or homologous tissues, with disappointing results. In an extensive analysis of the literature, Grillo [1] underlined the main technical difficulties and complications associated with the current surgical approaches to tracheal replacement. Complications associated with prosthetic grafts were mostly related to lack of biocompatibility and included local infection, anastomotic dehiscence, vascular erosion, granulomatous lesions, and stenosis. Complications associated with biologic tissues were related to the ischemic injury of the harvested graft leading to necrosis or stenosis. None of the proposed tracheal substitutes has produced consistent results that would standardize a clinical approach. In a preliminary study, we showed that partial or circumferential replacement of a limited tracheal segment using an autologous artery led to histologic transformation after few months into a structure resembling the tracheal tissue [2]. However, further studies were thought to be necessary to confirm these surprising findings and to investigate more extensive tracheal replacements for a longer period. This study reports the long-term clinical and histologic evolution up to 3 years of the replacement of long tracheal segments (5 cm) using an autologous aortic graft. This conduit was selected because of specific advantages such as similar diameter and resistance to infection. In addition, autologous tissue allowed us to avoid immunologic reactions, which could have obscured the observation.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Animals
Twenty-one sheep weighing 17 to 28 kg were used. The mean age of the animals was 3 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%, 8 mg/kg) and endotracheal intubation, ventilation was performed with a Siemens 900 C ventilator (tidal volume 10 mL/kg, 20 breaths/min). Anesthesia was maintained with inhaled 60% oxygen and 1% to 2% isoflurane. All animals were perfused with a crystalloid solution (10 mg · kg-1 · h-1). Arterial blood gases and pulse oximetry were monitored intraoperatively. Once awake, animals were immediately extubated. One gram of cefazolin was injected intramuscularly for 10 days after the operation.

Surgical procedure
The descending thoracic aorta was dissected through a left thoracotomy in the fifth intercostal space. Ligation and division of the left azygos vein was performed. After anticoagulation with heparin (0.5 mg/kg), an aortic shunt was placed between the transverse arch and the descending thoracic aorta at the level of the eighth intercostal space to avoid paraplegia. After cross-clamping the aorta and ligation of 4 to 10 intercostal arteries, a 5-cm-long segment of the descending thoracic aorta was resected circumferentially and replaced by a collagen polyester vascular prosthesis (Polythese; Laboratoire Perouse Implant, France) or a polytetrafluoroethylene (WL Gore and Associates, France) prosthesis using a running 4-0 polypropylene suture (Prolene; Ethicon, Inc, Somerville, NJ). The harvested thoracic aorta was placed in a heparinized blood and papaverine (4%) solution. The thoracic incision was closed over a thoracotomy drainage tube, which was removed at the time of extubation.

The cervical trachea was dissected through a median cervical incision. A 5-cm circular segment of the trachea, representing 9 to 11 cartilage rings, was resected. After insertion of a cross-field endotracheal tube into the distal tracheal segment to maintain ventilation, the harvested aortic autograft was interposed. Using distal intubation, the proximal end-to-end anastomosis and the posterior wall of the distal end-to-end anastomosis were made with a running 4-0 polydioxanone suture (PDS, Ethicon, Inc). After removal of the distal tube, the original endotracheal tube was guided back through the aortic autograft and inserted into the distal trachea. The distal anastomosis was then completed.

In 13 animals, an open knitted Ultraflex (Microvasive, Boston Scientific Corporation) stent (length, 8 cm; diameter, 14 mm) was placed in the lumen of the aortic graft under direct control and fiberscopic guidance to prevent collapse of the new airway. This uncovered stent is an open-ended cylindrical mesh constructed from a single strand of nitinol wire with the theoretical advantage of minimizing traumatic tissue compression, permitting ongoing mucociliary clearance while adapting to the anatomic contours. Because removal of the nitinol stent was impossible after 1 month, a removable Endoxane (Novatech) stent was used in 8 additional animals. Usually, this silicone stent is easily removed in humans and is considered as the standard prosthesis. Removal of the stent was performed under fiberscopic control at 1 (n = 2), 3 (n = 2), or 6 (n = 4) months.

Clinical evaluation
Clinical examination was performed daily until the tenth operative day, then monthly. Data on overall status, weight, respiratory status, and injury to the recurrent laryngeal nerve were collected. This evaluation included a fiberscopic examination (BFP 40, 10 mm; Olympus, France) under heavy sedation (propofol) at 1, 3, 6, 9, 12, 24, and 36 months to assess the viability of the aortic graft. The degree of graft stenosis was calculated from photographs and expressed as percentage reduction from normal trachea. Removal of granulations under bronchoscopic guidance to avoid stenosis has never been necessary. In addition, cervical and chest roentgenograms were performed at 1, 3, 6, 9, 12, 24, and 36 months to detect stent migration and pulmonary complications.

Histologic evaluation
Animals were sacrificed at 1, 3, 6, 9, 12, 24, and 36 months with an intravenous injection of potassium chloride and propofol to explant the grafts. En bloc resection of the trachea and the graft with surrounding tissues was performed and subjected to macroscopic and microscopic examinations. Postmortem specimens were immediately placed in a 10% formaldehyde solution for preservation. After removal of the tracheal stent and macroscopic evaluation of the graft, the specimens were embedded in paraffin, and 3-µm sections were submitted to hematoxylin eosin staining (HES) and orcein staining for light microscopy examination. Special attention was directed toward microscopic evidence of inflammation and morphologic transformation of the graft.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Results are presented in Table 1. All animals survived the operation with no paraplegia.


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  		Table 1. Type of Stent, Complications, Follow-Up, Bronchoscopic and Histologic Examinations

 
In the group with permanent stent (n = 13), three complications occurred. One animal died after an acute airway collapse as a result of displacement of the stent on postoperative day 2. One animal experienced an extensive laryngeal edema on postoperative day 7, and one had progressive dyspnea caused by an infected tracheal granuloma. These 2 animals were sacrificed 1 month after the operation. The remaining 10 animals had an uneventful recovery. Clinical status and chest roentgenograms were normal. Bronchoscopy showed no anastomotic leakage, graft rupture, or stenosis. The animals were sacrificed after 1 (n = 1), 3 (n = 3), 6 (n = 3), 9 (n = 1), and 12 months (n = 2) for histologic investigations.

In the group with temporary stent (n = 8), all animals had an uneventful postoperative course. In this group, clinical status and chest roentgenograms were normal, and bronchoscopy showed no anastomotic leakage, graft rupture, or stenosis. Attempts to remove the stent at 1 (n = 2) and 3 months (n = 2) led to airway collapse after 2 days and subsequently to death. In contrast, the 4 animals in which the stent was removed after 6 months did not show any respiratory impairment or stenosis with a 3-month to 30-month follow-up after removal.

The 19 tracheal specimens removed at different intervals after operation allowed us to follow the histologic evolution of the grafted aortic tissue. At 1 month, the usual histologic structure of the aorta had almost completely disappeared and was replaced by an extensive inflammatory tissue, a dense fibrosis, and scattered spots of nonkeratinizing metaplastic polystratified squamous epithelium. Islands of disorganized elastic fibers and immature cartilage were also observed within the fibrosis. At 3 months, a decrease in the intensity of the inflammatory process was observed with the appearance of cartilage and in 1 case a continuous mucociliary epithelium. After 6 to 12 months, this reparation process led to the formation of five to seven cartilage rings and continuous mucociliary epithelium (n = 3) or mixed epithelium (n = 6) comprising ciliated, secretory, and squamous cells. The specimen that was removed at 24 months showed a complete histologic transformation into a tracheal tissue with regular rings of newly formed cartilage, a posterior fibrous membrane, and a continuous mucociliary epithelium that has recovered its functional properties after removal of the stent (Figs 1–4). On the 3-year-old specimen, the total number of tracheal rings, including seven easily identified newly formed rings, did not differ significantly from the total number of rings counted on a control normal trachea: n = 48 versus 50 (Figs 5, 6). In addition, the intercartilaginous distance (normal average, 1 mm) was not significantly increased in the native area of the grafted tracheal specimen (Figs 7, 8), ruling out a significant contraction of the grafted area as healing progressed.



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  		Fig 1. Macroscopic view of a 24-month specimen showing the proximal and distal anastomoses (forceps) with new cartilage rings and the posterior membrane (bottom of the specimen).

 


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  		Fig 2. Histologic examination of the same specimen showing a continuous mucociliary epithelium (star) with an underlying dense connective tissue (asterisk) and cartilage neoformation (arrow).

 


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  		Fig 3. Histologic examination of the same specimen showing ciliated cells with apically numerous cilia (arrow) and goblet (mucus-secreting) cells (asterisk).

 


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  		Fig 5. Macroscopic views comparing a normal trachea (A) with a grafted trachea (B) removed en bloc 3 years after grafting (grafted area outlined by the rectangle). The total number of cartilage rings is similar in the two specimens (50 versus 48, respectively).

 


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  		Fig 4. Histologic examinations of the same specimen showing the cartilage tissue structure: extracellular matrix (asterisk) and chondrocytes (arrow).

 


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  		Fig 7. Extraluminal aspect of the grafted trachea showing the absence of retraction of the grafted area (rectangle) and the preserved intercartilaginous distances in the adjacent areas (arrow).

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
During the past 30 years, surgical techniques of tracheal resection and reconstruction by end-to-end anastomosis have been standardized to be performed in a variety of tracheal diseases such as stenosis, tracheomalacia, tuberculosis, traumatic injury, and malignancies. However, tracheal replacement using a tracheal substitute is necessary in extensive lesions. Numerous studies have been reported on the use of synthetic or biologic materials. The poor biocompatibility of synthetic materials led to major complications including infection, anastomotic leakage, granuloma, necrosis, stenosis, and erosion into major blood vessels [3, 4]. To improve biocompatibility, some authors have proposed the use of prosthetic materials conjugated with collagen or draped in omentum [5]. Several clinical trials have shown disappointing results [6, 7]. The first human tracheal homograft transplantation by Rose and colleagues [8] in 1979 offered a biologic alternative that seemed to be most promising. Encouraging medium-term results in children with recurrent tracheal stenosis have been observed after extensive tracheal homograft reconstruction using cadaveric transplant with temporary stenting [9]. However, the ischemic injury of the tracheal homograft as a result of devascularization led most commonly to necrosis and stenosis predominant in the middle area of the graft [10]. To prevent this complication, attempts were made to use vascularized tracheal homografts in animals with arterial and venous reconstruction [11]. Because of the complexity of the surgical procedure, no large clinical evaluation has emerged since these experimental studies. Attempts have been made with cryopreserved aortic homografts, but the short-term (14 days) results observed in only 10 rabbits did not permit any conclusion [12]. Another experimental study investigated tracheal reconstruction in rabbits using cryopreserved or fresh aortic homograft wrapped in a ringed, expanded polytetrafluoroethylene prosthesis [13]. The necrosis of the aortic graft observed in all animals was probably caused by the use of a prosthesis that has isolated the homograft from surrounding tissues and blood supply. Whatever the type of homograft used, the need for immunosuppression therapy does not favor the development of these surgical procedures in human. Autologous tissues do not present a risk of immunologic reaction and may be seen as ideal substitutes. Various autologous grafts have been evaluated in the past 50 years. Some authors have tried skin tubes supported by plastic rings [14]. Others evaluated urinary bladder wall: 4 months after the implantation of the graft, an osseous tissue with metaplastic epithelium was observed [15]. None of these grafts presented evidence of a functional trachea. The use of bowel or esophagus supported by a temporary stent has produced interesting results in animals [16, 17]. However, the harvest of esophagus is not without surgical risk in humans, and the diameter of the small bowel is not adequate. As far as we know, there has been no previous report on the use of autologous aortic tissue to replace the trachea. In preliminary studies, we showed that limited tracheal replacement using an autologous artery could lead to a histologic transformation into a structure resembling the tracheal tissue [2, 18]. We also showed that the placement of a stent in the lumen of the graft was necessary to avoid airway collapse and stenosis [19]. However, the resected tracheal segment measured a few centimeters, the number of animals studied was limited, and the length of follow-up was short.

The results of the present study show that extensive replacement of the trachea up to 5 cm with an autologous aortic graft could remain functional for long periods up to 3 years. Although we had shown in our preliminary study that stenting was necessary to avoid airway collapse, we did not know whether the stent should be removed and when. Two series of experiments, one with permanent stenting and the other with the stent removed at different intervals, allowed us to answer these questions. We found that stent removal is preferable to achieve a better recovery and function of the tracheal epithelium, but the removal should not be carried out before 6 months because early removal at 1 and 3 months led to airway collapse. After 6 months, the newly formed cartilage scaffold was able to prevent airway collapse. Stenting is also mandatory to avoid tracheal stenosis as shown by our previous experiments of partial anterior replacement of the trachea using an arterial patch without stent [2]. The permanent stent was well tolerated up to 6 months at which time a recurrent inflammatory process took place most likely because of the stent. This inflammation process led to a persistent metaplastic squamous epithelium and subsequently to unfavorable conditions for complete reparation of the epithelium. An important finding was the fact that bronchoscopic examinations showed no anastomotic leakage, no graft rupture, and no stenosis except for 1 animal that had an infected tracheal granuloma at 1 month. The more intriguing aspects of this study are the histologic findings. They revealed an unexpected capacity of transformation of the autologous aortic graft into tracheal tissue whenever placed in the tracheal environment. Animals were in good condition at the time of sacrifice, and histologic examinations of the graft at different intervals found no evidence of necrosis or ischemia. At 1 month, the usual arterial framework had almost completely disappeared and was replaced by an extensive inflammatory process associated with fibrosis. Between 1 and 3 months, the inflammatory process regressed with the appearance of a squamous epithelium and cartilage formation. Beyond 3 months, some secretory and ciliated cells appeared in scattered areas. A continuous mucociliary epithelium was found at 3 months in 1 case of the group with permanent stent and in the 4 cases that had removal of the stent after 6 months. The newly formed cartilage was found in all specimens beyond 1 month. Cartilage rings developed in the anterior wall of the graft with an anatomically correct posterior membrane after 3 months.

The question arises whether these cartilage rings were actually newly formed rings or native rings displaced toward the reconstructed tracheal area by a process of contraction as healing progressed. Previous experiments by Pressman [20] seem to support this last hypothesis. Using a polyethylene tube that was telescoped into each end of a resected segment of the trachea, the author found a neoformation of a circumferential fibrous tissue wrapping the tube followed by a longitudinal contraction of this tissue. This newly formed tube was lined with epithelium in some cases, but no cartilage ring neoformation was observed because of either the different experimental conditions or a follow-up limited to a few weeks. The mechanism of contraction of the grafted area can be excluded in our own series because the number of cartilage rings was similar in a grafted specimen and a control specimen. In addition, the intercartilaginous distance was not modified in the native trachea (Figs 5–8) as seen not only in the 3-year specimen but also in specimens beyond 6 months. The only difference between grafted tracheas and the normal trachea was that cartilage rings were not as regular as normal rings.



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  		Fig 6. Roentgenograms of the same two specimens as in Figure 5 showing the absence of stenosis of the grafted area and the continuity of the tracheal walls. Spots of calcification are visible.

 


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  		Fig 8. Intraluminal aspect of the grafted trachea showing the absence of retraction of the grafted area (rectangle) and the preserved intercartilaginous distances in the adjacent areas (arrow).

 
These findings raise the question of how the aortic tissue can transform into an almost normal trachea within 6 months. As far as epithelial regeneration is concerned, previous studies on cellular regeneration after epithelial injury can help us understand the mechanisms involved [21]. The tracheal epithelium is composed of three types of cells: basal, secretory, and ciliated cells. The latter represent the final stage of cellular maturation [22]. The origin of the cells promoting the epithelial reconstruction remains unclear [23, 24]. Some authors have demonstrated that migration, proliferation, and differentiation of basal and secretory cells into ciliated cells led to regeneration of an epithelium after experimental injury of the tracheal epithelium similar to the epithelial formation observed during the fetal stage [25]. The common hypothesis proposed by most authors is the migration of basal and mucus cells into the destroyed area followed by formation of a mucociliary epithelium after a transitory stage of a metaplastic epithelium. More difficult is to explain the transformation of the vascular tissue into cartilage rings and a well-organized fibrous tissue of the membranous posterior wall. Taking into consideration the close relationship between respiratory epithelium and its underlying substructure [26], we can hypothesize that the inflammatory response created favorable conditions for reepithelialization and subsequent cartilage neoformation from stem cells triggered by environmental factors, which must be identified. The interaction between cells and cartilage is further supported by the fact that cartilage regulates the expression of growth factors, which could stimulate and regulate cell proliferation and differentiation [26].

In conclusion, this study confirms that an autologous aortic graft is a valuable substitute for extensive tracheal replacement. It does show that a stent is needed for a minimal period of 6 months and should be removed afterward for a complete regeneration of the epithelium. It also shows a progressive transformation of the vascular graft into a structure resembling the tracheal tissue. This transformation was responsible for the long-term patency of the trachea and its normal function up to 3 years. In humans, the use of the subrenal segment of the abdominal aorta would be preferred because of the appropriate diameter and the practical difficulties of harvesting and reconstructing a thoracic segment. The use of an arterial allograft would be more practical, but it remains to be demonstrated that the same tracheal neogenesis and the same long-term function can be obtained in spite of the allogeneic nature of the graft.

This work was supported by a grant from the University Pierre et Marie Curie of Paris and by The Alain Carpentier Foundation. Doctor Emmanuel Martinod received The Alain Carpentier Foundation Award in 2000.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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  10. Lenot B., Macchiarini P., Dulmet E., Weiss M., Dartevelle P.H. Tracheal allograft replacement: an unsuccessful method. Eur J Cardiothorac Surg 1993;7:648-652.[Abstract]
  11. Macchiarini P., Mazmanian G.-M., de Montpréville V., et al. Experimental tracheal and tracheoesophageal allotransplantation. J Thorac Cardiovasc Surg 1995;110:1037-1046.[Abstract/Free Full Text]
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  19. Martinod E., Zegdi R., Zakine G., et al. A novel approach to tracheal replacement: the use of an aortic graft. J Thorac Cardiovasc Surg 2001;122:197-198.[Free Full Text]
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Ann. Thorac. Surg., March 1, 2005; 79(3): 942 - 948.
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N. J. Demos
Tracheal Ring Regeneration
Ann. Thorac. Surg., October 1, 2004; 78(4): 1511 - 1511.
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E. Martinod and A. F. Carpentier
Reply
Ann. Thorac. Surg., October 1, 2004; 78(4): 1511 - 1511.
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H. Mertsching, T. Walles, and P. Macchiarini
Replacement of the trachea with an autologous aortic graft
Ann. Thorac. Surg., September 1, 2004; 78(3): 1132 - 1133.
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E. Martinod and A. F. Carpentier
Replacement of the trachea with an autologous aortic graft: Reply
Ann. Thorac. Surg., September 1, 2004; 78(3): 1133 - 1133.
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M. G. Hazekamp and N. Nijdam
Use of autologous arterial patches for tracheal reconstruction in young infants
Ann. Thorac. Surg., June 1, 2004; 77(6): 2262 - 2263.
[Full Text] [PDF]

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