Ann Thorac Surg 2005;79:942-948
© 2005 The Society of Thoracic Surgeons
Original article: General thoracic
Tracheal Regeneration Following Tracheal Replacement With an Allogenic Aorta
Emmanuel Martinod, MD, PhDa,b,*,
Agathe Seguin, MDa,b,
Muriel Holder-Espinasse, MDc,
Marianne Kambouchner, MDd,
Martine Duterque-Coquillaud, PhDc,
Jacques F. Azorin, MDb,
Alain F. Carpentier, MD, PhDa
a Laboratoire d'Etude des Greffes et Prothèses Cardiaques, Hôpital Broussais, Université Paris 6, Paris, France
b Service de Chirurgie Thoracique et Vasculaire, Hôpital Avicenne, Université Paris 13, Paris, France
d Service d'Anatomo-Pathologie, Hôpital Avicenne, Université Paris 13, Paris, France
c Institut de Biologie, Lille, France
Accepted for publication August 3, 2004.
* Address reprint requests to Dr Martinod, Laboratoire d'Etude des Greffes et Prothèses Cardiaques, Hôpital Broussais, Pavillon René Leriche, 96 rue Didot, 75674 Paris Cedex 14, France (E-mail: emartinod{at}wanadoo.fr).
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Abstract
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BACKGROUND: Tracheal replacement remains an unsolved surgical problem. Attempts to use tracheal substitutes have failed to achieve reliable results. In this study, tracheal regeneration was obtained after tracheal replacement with an allogenic aorta.
METHODS: Twenty female sheep underwent a 8-cm tracheal replacement with a fresh aortic allograft. In the six last animals, aortic grafts came from male sheep. A stent prevented airway collapse. No immunosuppressive therapy was used. Aortic segments were retrieved at regular intervals up to 16 months. A polymerase chain reaction for the SRY gene was performed in specimens with aortic grafts from male sheep.
RESULTS: All animals but one survived the operation without complications. Clearly identified between the suture lines, the aortic segments were completely transformed into a tracheal structure. Histology showed initially an inflammatory reaction with proliferation of a squamous epithelium followed by mucociliary epithelium and newly formed cartilage rings. SRY gene was not found in newly formed cartilage rings showing that the regeneration originated from recipient cells.
CONCLUSIONS: This study presents a new type of tissue regeneration and brings hopes to the treatment of extensive tracheal lesions.
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Introduction
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Most tracheal lesions can be treated by tracheal resection followed by mobilization and reconstruction of the remaining tracheal segments by end-to-end anastomosis. Whenever extensive lesions involve more than half of the tracheal length in adult or more than one third in children, primary reconstruction is not possible. Patients with these lesions are treated with palliative techniques namely irradiation and stents or T tubes. In the past 60 years major advances in medicine allowing for successful replacement of organs as complex as heart, lungs, liver or kidneys have advanced while, at the same time, attempting to replace the trachea, a rather simple conduit for the passage of air, have failed. The various tracheal substitutes and techniques of reconstruction were recently analyzed by Grillo [1], who classified them in five categories: foreign materials, nonviable tissues, autogenous tissues, tissue engineering, and tracheal transplantation. Attempts with foreign materials led to problems of chronic infection, airway obstruction, migration of the prosthesis, erosion of major blood vessels and proliferation of granulation tissue. Implantation of nonviable tissues, either chemically treated, frozen or lyophilized has been associated with poorly functional results. Reconstructions with autogenous tissues such as skin, fascia lata, pericardium, costal cartilage, bladder, esophagus or bowel are complex procedures, which have been associated with disappointing results. More recently, efforts have been made to induce the formation of cartilaginous tubes covered with epithelial cells, but to date this type of tissue engineering has not provided reliable results. Finally, tracheal allotransplantation has been also disappointing so far due to complication of necrosis or stenosis of the graft. In addition immunosuppressive therapy does not permit a clinical application in the treatment of cancer. As Grillo suggested : "We must continue to maintain an open mind about this intriguing but thus far unsolved surgical dilemma - replacement of the tracheal conduit" [2].
In a previous work, we investigated living autologous aortic conduit to avoid immunologic reactions [3]. Instead of the expected successful grafting of the aorta, we actually found an inflammatory reaction leading to the destruction of the aortic tissue and its progressive replacement by a tracheal structure with mucociliary epithelium and newly formed cartilage. This technique, however, had a limited value in clinical practice because of the need to remove an aortic segment from the patient himself with the risk of paraplegia. An aortic allograft would be a better practical solution, but potential problems of immunologic reaction could compromise the results. In addition, it was doubtful that the transformation observed with an autologous tissue would be reproducible with an allogenic tissue. The experimentation reported in this study has been carried out to address these questions.
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Material and Methods
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Tracheal replacement with a fresh aortic allograft was performed in 20 female sheep. In order to avoid possible confusion with a simple process of repair by contraction of the conduit and extension of the remaining tracheal segments, 8-cm tracheal resections were carried out instead of the 5-cm in our previous experiments. The aortic segment was taken from female sheep for the first 14 animals and from male sheep for the 6 remaining animals. The transplantation of male aorta to female recipient allowed us to analyze the newly formed tissues, especially the cartilage using polymerase chain reaction (PCR) technique for detection of the SRY gene.
Animals
Thirty sheep weighing 24 to 30 kg were used. The mean age of the animals was 4 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.
Harvest of the Aortic Allografts
Two 8-cm circular segments of the descending thoracic aorta were harvested through a left thoracotomy in 10 sheep. The harvested grafts were placed in a heparinized blood and papaverine (4%) solution for 2 to 5 hours and then transplanted. The harvested grafts came from female donors for the 7 first animals and from male donors for the 3 remaining animals.
Anesthesia, Surgical Procedure, and Clinical Evaluation
In 20 female sheep, induction of anesthesia was made using intravenous propofol (1%, 8 mg/kg). After endotracheal intubation, ventilation was performed with a Siemens 900C ventilator (tidal volume 10 mL/kg, 20 breaths/min; Siemens Medical Systems, Inc., Iselin, NJ). 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). The cervical trachea was dissected trough a median cervical incision. A 8-cm circular segment of the cervical trachea, representing 15 to 17 cartilage rings, was resected. After insertion of a cross-field endotracheal tube into the distal tracheal segment to maintain ventilation, the harvested aortic allograft 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, Sommerville, NJ). After removal of the distal tube, the original endotracheal tube was guided back trough the aortic allograft and inserted into the distal trachea. The distal anastomosis was then completed. In all animals, a silicone Endoxane (Novatech) stent (length = 11 cm, diameter = 15 mm) was placed in the lumen of the aortic graft under direct control and bronchoscopic guidance to prevent collapse of the new airway. The cervical incision was then closed with no drainage. Once awake, animals were immediately extubated. One gram of cefazolin was injected intramuscularly for 10 days after the operation. No immunosuppressive therapy was given. Clinical examination was performed daily until the tenth operative day, then monthly. Data on overall status, weight and respiratory status were collected. The postoperative evaluation included a fiberscopic examination (BPF 40, 10 mm, Olympus, France) under heavy sedation using propofol at 1, 3, and 6 months to assess the patency of the airways. The degree of graft stenosis was calculated after removal of the stent at the time of sacrifice, and was expressed as percentage reduction from normal trachea.
Histologic Examinations
Animals with an aortic graft from female sheep were sacrificed at 1 (n = 3), 3 (n = 3), 6 (n = 3), 12 (n = 3), and 16 (n = 1) months with an intravenous injection of potassium chloride and propofol in order to explant the grafts. Animals with an aortic graft from male sheep were sacrificed at 2 (n = 2), 5 (n = 2), and 7 (n = 2) months using the same protocol. En bloc resection of the trachea and the graft with surrounding tissues was performed and subjected to macroscopic and microscopic examinations. After removal of the tracheal stent and macroscopic evaluation of the graft, the postmortem specimens were immediately placed in a 10% formaldehyde solution for preservation. The specimens were embedded in paraffin, and 3-µm sections were submitted to hematoxylin-eosin staining (HES) for light microscopy examination. Aortic grafts were submitted to in situ RNA hybridization with radioactive RNA for type II collagen. For animals with an aortic graft from male sheep, the half of the specimens was frozen at –80°C for the following study.
PCR for the SRY Gene on Cartilage
SAMPLES
Tracheal samples were available from male and female control sheep, as well as from female tracheal specimens explanted 7 months (n = 2) after transplantation of a male aortic allograft. Cartilage rings from control sheep and newly formed cartilage rings from the grafts were dissected (0.5 to 1 cm) for DNA analysis.
DNA EXTRACTION FROM CARTILAGE SAMPLES
Total DNA was extracted according to the following protocol. Cartilage samples were incubated overnight at 56°C with proteinase K and DNA was extracted by classic phenol/chloroform technique.
PCR FOR THE SRY AND INSULIN-LIKE GROWTH FACTOR 1 GENES
We carried out amplification for the SRY gene on each sample (male trachea, female trachea, graft). As a tracer for the DNA extraction and amplification steps, we used primers for insulin-like growth factor 1 (IGF1) gene as a positive control (Table 1). Amplification was carried out in a Perkin-Elmer instrument (Perkin-Elmer, Norwalk, CT). PCR was set up in a final volume of 50 µL, with 29 pmol of each primer, 10x Taq polymerase buffer, 0.75 mmol/L of magnesium chloride, 200 µmol/L dNTPs, 2.5 U of Taq polymerase, and 5 µL of extracted DNA (ie, 50 ng/µL). The PCR products were 114 base pairs (bp) for SRY and 116 bp for IGF1. The thermal cycling was as follows: denaturation at 95°C for 10 minutes, followed by 40 cycles of 95°C for 30 seconds, 53°C for 30 seconds, and 72°C for 10 seconds with final incubation at 72°C for 10 minutes. In the case of negative results for SRY gene amplification, the presence of correct amplification of the IGF1 gene was checked. Positive results in this PCR demonstrate the efficiency of the process and validate any negative result for SRY gene detection.
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Results
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Clinical Evaluation
The postoperative course was uneventful in all cases (Table 2). One animal died at 2 months. Postmortem examination found no anomaly or complication of the reconstructed trachea. In all other animals, clinical evaluation showed no anastomotic leakage, no dehiscence and no stenosis for periods of follow up extending from 1 to 16 months. Although being in excellent condition the animals were sacrified at regular intervals to follow the histologic transformation.
Pathology Findings
Macroscopic examination confirmed the absence of stenosis in all specimens (Fig 1 and Table 2). After removal of the stent, the tracheal conduit showed a regular inner surface without ulceration or granulomatous proliferation. Careful measurements of the distance between the upper anastomosis and the lower anastomosis of the aortic segments revealed an average 2.7-cm longitudinal contraction (extremes = 1.6 to 3.3 cm) with an easily identified 4.7 to 6.4 cm neotrachea between the two suture lines. Microscopic examinations revealed a progressive transformation of the aortic tissue into a tracheal tissue comprising an epithelium and newly formed cartilage (Fig 2).
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Fig 1. Macroscopic view of a neotrachea at 12 months showing the absence of stenosis. The two suture lines (arrows) delineate the regenerated trachea, the new cartilage rings, and the continuous epithelium.
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Fig 2. Histologic examination at 3 months showing a continuous epithelium with islands of newly formed cartilage (stars) (hematoxylin-eosin staining, original magnification x50).
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At 1 and 2 months (n = 5), a major inflammatory reaction was observed with a predominance of lymphocytes. In all five animals, a nonkeratinizing metaplastic polystratified squamous epithelium was visible. The epithelium was continuous in 3 or interrupted in 2 (Fig 3). Newly formed islands of immature cartilage were seen in 4 specimens.
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Fig 3. Histologic examination at different stage of follow-up from 1 to 12 months shows the successive steps of epithelium regeneration from squamous (a, b) to mixed (c), and to mucociliary (d) (hematoxylin-eosin staining, original magnification x200).
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At 3, 5, 6, and 7 months (n = 10), newly formed cartilage took the aspect of immature cartilage in 6 cases and of regular cartilage rings in 4 cases (Fig 4). The epithelium was mixed (n = 7), squamous (n = 1), or mucociliary (n = 2) (Fig 3). The inflammatory reaction was less important (n = 10).
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Fig 4. Histologic examination at 3 months showing islands of newly formed immature cartilage (stars) within the aortic allograft (hematoxylin-eosin staining, original magnification x200).
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At 12 and 16 months (n = 4), newly formed vascularized cartilage rings were observed in all cases (Fig 5). The epithelium was continuous and either mixed (n = 3) or mucociliary (n = 1). There was no sign of inflammation.
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Fig 5. Histologic examination at 12 months showing a vascularized mature newly formed cartilage (hematoxylin-eosin staining, original magnification x200).
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Disorganized aortic elastic fibers observed in all 19 specimens progressively disappeared as the length of follow-up increased (Fig 6).
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Fig 6. Histologic examination at 3 months showing disorganized elastic fibers (arrows) from the aortic allograft (hematoxylin-eosin staining, original magnification x100).
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In situ RNA hybridization was positive for type II collagen in newly formed cartilage (Fig 7).
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Fig 7. In situ RNA hybridization with radioactive RNA was positive (white spots) for type II collagen in newly formed cartilage at 7 months.
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PCR for the SRY Gene on Cartilage
In two female specimens with male aortic segments removed after 7 months, a PCR for the SRY gene was performed on newly formed cartilage (Fig 8). Sex prediction on the SRY gene PCR assay revealed positive results for cartilage samples from a male control sheep. All the other samples from a female control sheep and from the aortic graft were negative for SRY amplification. IGF1 amplification was positive in each cartilage sample.
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Fig 8. SRY and IGF1 genes amplification on 3% acrylamide gel. SRY gene is not expressed in the graft specimen. (IGF1 = insulin-like growth factor 1; PHA = phytohemagglutinin; SRY = SRY gene.)
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Comment
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Although most organs are successfully transplanted to date, the trachea remains an exception. Tracheal replacement with prosthesic or biological substitutes such as allografts or autologous grafts (trachea, esophagus, bowel, skin, or bladder) did not provide results satisfactory enough to lead to clinical application [4–16]. In a previous work, we reported that an autologous aortic segment could be a valuable substitute to the trachea for periods up to 3 years [3, 17, 18]. In 4 animals, the stent used to avoid airway collapse could be removed after 6 months. No complication was noticed in the following 3 months in 2 animals, 18 months in 1 animal, and 30 months in 1 animal. This method however could not have a significant impact in surgical practice because of the need to replace the harvested aortic segment by a vascular prosthesis with the risk of paraplegia due to devascularization of the spinal cord. In addition, the use of 5-cm segments in this early experiment led to question wether the neotrachea was the result of the contraction of the transplanted conduit and spontaneous repair by extension of the two remaining segments. The results however were surprising enough to further explore this process of tracheal regeneration using longer aortic segments up to 8-cm taken from another animal. In order to implant a viable tissue, we preferred to use fresh aortic allografts instead of chemically treated, frozen or lyophilized aortas. As suggested by major clinical studies about the use of aortic allografts in vascular surgery, we chose not to give immunosuppressive therapy [19]. We report for the first time here that allogenic aortic segments implanted in the tracheal environment after extensive tracheal resection were replaced after few months by a new trachea comprising mucociliary epithelium, cartilage rings and a posterior membrane. The process observed here differs from the process of successful grafting since the transplanted tissue disappeared completely. Successful grafting of aortic allografts has been observed following replacement of segments of abdominal or thoracic aorta. They were shown to keep their original histologic structure despite some discrete immunologic reaction [19–21]. In our study, the aortic tissue lost its original structure completely, probably as a result of ischemia since contrary to a vascular graft the aortic segment was not in contact with circulating blood. The ischemia of the aortic tissue led to an intense inflammatory reaction, which together with the creeping extension of the epithelium played a major intermediary role in the process of tracheal regeneration. The regeneration of the epithelium, which comprised squamous and mucociliary areas, was not a surprise because it has been well documented after elective destruction of the tracheal epithelium or replacement using homografts or autografts [15, 16, 22–26]. The same reparative process was observed here, but in addition we found newly formed cartilage rings that have never been observed previously with any other biological substitutes. The litterature reports only two studies in which an aortic allograft had been used to replace the trachea but in none of them the formation of cartilage had been observed [27, 28]. This difference with our findings can be explained by a shorter follow-up (14 days) in the first study and different experimental conditions in the second study with the aorta placed within a prosthesis to protect the aortic tissue from the inflammatory response. Therefore, we can postulate that the environment plays a major role to induce tissue transformation leading toward a structure as complex as a trachea with cartilage rings and posterior membrane. 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 others seem to support this last hypothesis [29–31]. In our own series, the measurements of the distance between the two suture lines clearly showed that contraction was a minor process (one third of the total length of the resected area). Furthermore, the mechanism of a complete contraction of the 8-cm aortic grafts can be excluded because we observed regenerated cartilage not only in the area of the sutures but also in the middle of the replaced segment. Most importantly, we found newly formed cartilage at each stage of maturation (from immature islands of chondrocytes to mature cartilage) recapitulating the process of cartilage formation during the embryologic period. It remained to be found, however, where this cartilage came from. Using PCR technique and chromosome Y identification in female sheep having received a male aorta, we could demonstrate that the cartilage cells derived from the recipient most probably were mesenchymatous cells triggered by local signals of differentiation. The fact that chondrocytes are not known as cells capable to migrate weakens the hypothesis of a distant migration from the tracheal remnants. The fact that the cartilage observed in this study was identified as young cartilage reinforces this statement. The role of stem cells and progenitor cells has been shown for in situ regeneration of destructed areas of tissues or organs such as heart, liver, brain, kidneys or more recently trachea, but here we were faced with a different process since another tissue (the aorta) playing an intermediary role was necessary to facilitate the regeneration that did not occur with serious attempts [32–35].
In this experiment, the transformation of the aortic tissue into a tracheal tissue was most probably induced by environmental factors. Tissue transformation can also be obtained at the molecular end by physical factors such as electrical stimulation for example [36, 37]. Whatever the means used, induced tissue transformation may open the way to important clinical applications. In humans, the use of a fresh aortic allograft instead of a nonviable aorta from a tissue bank could be preferable in order to induce the transformation of the aortic graft into a tracheal tissue. However, this has to be confirmed by a new phase of experiments evaluating the use of cryopreserved or fixed aortic grafts.
In conclusion, this study demonstrated that the transplantation of an allogenic aortic segment to replace a segment of the trachea led to a complete regeneration of a tracheal structure including tracheal cartilaginous rings while the aortic tissue disappeared completely. Knowing the interaction between tracheal epithelium and cartilage, we can postulate that the epithelium extending from the remaining tracheal tissue expressed factors, which stimulated the regeneration of cartilage. Most striking was the fact that the newly formed cartilage was able to reconstruct almost normal tracheal rings and a posterior membrane. This study not only underlines the diversity of the tissue transformation processes but also brings new hopes to the unsolved problem of tracheal replacement in humans.
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Acknowledgments
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The authors thank Nathalie Goussef, Martine Rancic, and Cyril Schneider-Maunoury for their valuable technical assistance.
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D. M. Radu, A. Seguin, P. Bruneval, A. Fialaire Legendre, A. Carpentier, and E. Martinod
Bronchial Replacement With Arterial Allografts
Ann. Thorac. Surg.,
July 1, 2010;
90(1):
252 - 258.
[Abstract]
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A. Wurtz
Tracheal Replacement With Banked Cryopreserved Aortic Allograft
Ann. Thorac. Surg.,
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H. Tsukada, A. Ernst, S. Gangadharan, S. Ashiku, R. Garland, D. Litmanovich, and M. DeCamp
Tracheal Replacement With a Silicone-Stented, Fresh Aortic Allograft in Sheep
Ann. Thorac. Surg.,
January 1, 2010;
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253 - 258.
[Abstract]
[Full Text]
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D. Makris, M. Holder-Espinasse, A. Wurtz, A. Seguin, T. Hubert, S. Jaillard, M. C. Copin, R. Jashari, M. Duterque-Coquillaud, E. Martinod, et al.
Tracheal Replacement With Cryopreserved Allogenic Aorta
Chest,
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60 - 67.
[Abstract]
[Full Text]
[PDF]
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M. B. Davidson, K. Mustafa, and R. W. Girdwood
Tracheal Replacement With an Aortic Homograft
Ann. Thorac. Surg.,
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88(3):
1006 - 1008.
[Abstract]
[Full Text]
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D. Fabre, S. Singhal, V. De Montpreville, B. Decante, S. Mussot, O. Chataigner, O. Mercier, F. Kolb, P. G. Dartevelle, and E. Fadel
Composite cervical skin and cartilage flap provides a novel large airway substitute after long-segment tracheal resection
J. Thorac. Cardiovasc. Surg.,
July 1, 2009;
138(1):
32 - 39.
[Abstract]
[Full Text]
[PDF]
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A. Seguin, D. Radu, M. Holder-Espinasse, P. Bruneval, A. Fialaire-Legendre, M. Duterque-Coquillaud, A. Carpentier, and E. Martinod
Tracheal Replacement With Cryopreserved, Decellularized, or Glutaraldehyde-Treated Aortic Allografts
Ann. Thorac. Surg.,
March 1, 2009;
87(3):
861 - 867.
[Abstract]
[Full Text]
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A. Maciejewski, C. Szymczyk, S. Poltorak, and M. Grajek
Tracheal Reconstruction With the Use of Radial Forearm Free Flap Combined With Biodegradative Mesh Suspension
Ann. Thorac. Surg.,
February 1, 2009;
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608 - 610.
[Abstract]
[Full Text]
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H. Tsukada, S. Matsuda, H. Inoue, Y. Ikada, and H. Osada
Comparison of bioabsorbable materials for use in artificial tracheal grafts
Interact CardioVasc Thorac Surg,
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225 - 229.
[Abstract]
[Full Text]
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T. Sato, H. Tao, M. Araki, H. Ueda, K. Omori, and T. Nakamura
Replacement of the Left Main Bronchus With a Tissue-Engineered Prosthesis in a Canine Model
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422 - 428.
[Abstract]
[Full Text]
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A. Abbasidezfouli, M. B. Shadmehr, M. Arab, M. Javaherzadeh, S. Pejhan, A. Daneshvar, and R. Farzanegan
Postintubation Multisegmental Tracheal Stenosis: Treatment and Results
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[Abstract]
[Full Text]
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D. Galetta and L. Spaggiari
Tracheal Reconstruction for a Long Tracheal Resection
Ann. Thorac. Surg.,
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[Full Text]
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A. Ernst and S. Ashiku
Tracheal Transplantation: Are We Any Closer to the Holy Grail of Airway Management?
Chest,
November 1, 2006;
130(5):
1299 - 1300.
[Full Text]
[PDF]
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S. Jaillard, M. Holder-Espinasse, T. Hubert, M.-C. Copin, M. Duterque-Coquillaud, A. Wurtz, and C.-H. Marquette
Tracheal Replacement by Allogenic Aorta in the Pig
Chest,
November 1, 2006;
130(5):
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[Abstract]
[Full Text]
[PDF]
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A. Seguin, E. Martinod, M. Kambouchner, G. O. Campo, P. Dhote, P. Bruneval, J. F. Azorin, and A. Carpentier
Carinal Replacement With an Aortic Allograft
Ann. Thorac. Surg.,
March 1, 2006;
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[Abstract]
[Full Text]
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J. F. Azorin, F. Bertin, E. Martinod, and M. Laskar
Tracheal replacement with an aortic autograft
Eur J Cardiothorac Surg,
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[Abstract]
[Full Text]
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Top
Abstract
Introduction
