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Ann Thorac Surg 2010;90:252-258. doi:10.1016/j.athoracsur.2010.03.079
© 2010 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Bronchial Replacement With Arterial Allografts

Dana M. Radu, MDa,b, Agathe Seguin, MDa,b, Patrick Bruneval, MD, PhDc, Anne Fialaire Legendre, MDd, Alain Carpentier, MD, PhDb,*, Emmanuel Martinod, MD, PhDa,b,*,*

a Département de Chirurgie Thoracique et Vasculaire, Assistance Publique-Hôpitaux de Paris, Hôpital Avicenne, Université Paris XIII, Faculté de Medecine SMBH, Bobigny, France
b Université Paris Descartes, EA Laboratoire de Recherches Biochirurgicales, Assistance Publique-Hôpitaux de Paris, Hôpital Européen Georges Pompidou, Paris, France
c Département d'Anatomopathologie, Assistance Publique-Hôpitaux de Paris, Hôpital Européen Georges Pompidou, Université Paris Descartes, Faculté de Médecine, Paris, France
d Etablissement Français du Sang Ile de France, Banque de Tissus, Assistance Publique-Hôpitaux de Paris, Hôpital Henri Mondor, Créteil, France

Accepted for publication March 11, 2010.

* Address correspondence to Dr Martinod, Département de Chirurgie Thoracique et Vasculaire, Pôle Hémato-Onco-Thorax, Assistance Publique-Hôpitaux de Paris, Hôpital Avicenne, 125 rue de Stalingrad, 93009 Bobigny, France (Email: emmanuel.martinod{at}avc.aphp.fr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Background: Pneumonectomy is well known for a high risk of postoperative death. The alternative, sleeve lobectomy, is sometimes technically inaccessible, and is associated with locoregional recurrence. In certain situations, the use of a bronchial substitute would allow longer bronchial resections with better security margins. Previous experiments demonstrated that aortic grafts are valuable tracheal and carinal substitutes. The present study evaluated bronchial replacement with arterial allografts.

Methods: Fifteen female sheep underwent a left bilobectomy with replacement of the bronchus intermedius with arterial allografts: 5 received a fresh graft (group 1) and 10 received cryopreserved (group 2). A bronchial silicone stent was used to confer rigidity. Evaluation was conducted on clinical and histologic criteria at regular intervals up to 18 months.

Results: There were no perioperative deaths. Atelectasis, the only early postoperative complication (n = 2), was successfully treated by fiberscopic aspiration. The late postoperative period was uneventful in 12 sheep. Complications included 1 bronchopneumonia, 1 pulmonary abscess, and 1 distortion of the bronchial stent. Fiberscopic examination revealed 3 sheep with granuloma formation. The bronchial stent was removed in 3 sheep, 1 at 9 months and 2 at 12 months, without clinical complications or stenosis of the graft. Histologic analysis showed regeneration of new bronchial tissue, comprising epithelium and cartilage.

Conclusions: This study confirmed that an arterial allograft could be a valuable bronchial substitute. The use of a bronchial substitute offers new perspectives in surgical resection of lung cancer because it would avoid pneumonectomy in some patients.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Survival is the main concern for patients operated on for non-small cell lung cancer. Although lobectomy has an acceptable postoperative mortality of 2.9% [1] even after induction therapy [2], pneumonectomy has a high mortality rate of up to 23.9% after induction therapy [2–4]. Pneumonectomy is also associated with an increased risk of long-term cardiopulmonary complications [5], with a negative influence on quality of life and long-term survival [6].

An established alternative to pneumonectomy is sleeve lobectomy, a technique that allows the preservation of pulmonary parenchyma and consequently offers better quality of life [6]. Nevertheless, sleeve lobectomy has raised controversies because it is thought to be more prone to local recurrence than pneumonectomy [6]. The use of this technique is sometimes difficult, and its completion needs the adjunct of another challenging procedure, such as a pulmonary artery resection [7] or a bronchoplastic segmentectomy [8]. Further resection of a microscopically invaded bronchial stump is sometimes unfeasible because the bronchial ends are too remote to perform a safe tension-free anastomosis, and so surgeons abandon the procedure in favor of a pneumonectomy.

In certain situations therefore, a bronchial substitute would be advantageous to facilitate sleeve resection. Its elective use could offer a more anatomic reconstruction of the airway. It would permit longer bronchial resections with better security margins, thus reducing the risk of locoregional recurrence and the necessity to perform a pneumonectomy.

In previous research, we demonstrated that aortic grafts are valuable tracheal and carinal substitutes that allow regeneration of epithelium and cartilage [9–13]. Therefore, in the present study, we evaluated the use of arterial allografts as bronchial substitutes to determine the feasibility and the possible complications of the procedure and to assess the transformations of the arterial allograft in a bronchial position and the differences between the use of a fresh and a cryopreserved allograft.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Animals
All animals used in this study received care in compliance with the Guide for the Care and Use of Laboratory Animals (Institute of Laboratory Animal Resources, National Research Councils; National Academy Press, revised 1996). The study used 15 female sheep with a mean weight of 37 kg (range, 30 to 43 kg) and a mean age of 6.5 months (range, 5 to 9 months).

Harvest and Preservation of Arterial Allografts
The ascending aortas, common brachiocephalic trunks, and descending aortas were harvested in 4 female sheep. The arteries were divided in fragments of about 2.5 cm and then underwent the preservation procedure. Two preservation methods were used: fresh preservation and cryopreservation (see Appendix for details).

Experimental Design
Animals were assigned to one of the two groups: group 1 (n = 5) underwent replacement of the left bronchus intermedius with a fresh arterial allograft; group 2 (n = 10) underwent replacement of the left bronchus intermedius with a cryopreserved arterial allograft.

The left lung in sheep has 3 lobes. Distal to the origin of the apical lobe bronchus, the primary bronchus becomes the bronchus intermedius. After a short distance, it divides into cardiac lobe bronchus and diaphragmatic lobe bronchus.

Surgical Procedure
The procedure was conducted under general anesthesia and tracheal intubation (see Appendix for details). A left posterolateral thoracotomy was performed, and the intercostal muscle of the fifth intercostal space was harvested. To obtain adequate exposure of the left bronchus intermedius, a bilobectomy of the apical and cardiac lobes was performed.

The left main bronchus was clamped, and a bronchial segment of the bronchus intermedius was resected (sometimes including the two lobar bronchial stumps, depending on the anatomic configuration). An arterial allograft about 15 mm long was interposed by 2 running sutures of 5-0 polydioxanone (Fig 1A). In length, the grafted segment represented about 75% of the sum of lengths of the primary bronchus and bronchus intermedius.


Figure 1
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  		Fig 1. Intraoperative views: (A) Bronchial replacement with an arterial allograft. The clamp is on the main left bronchus. (B) This view of bronchial replacement shows the nonabsorbable suture used to secure the bronchial stent.

 
First the distal anastomosis and the posterior wall of the proximal anastomosis were performed. Under direct vision, a removable bronchial silicone stent (Tracheobroxane Dumon BD, Novatech, La Ciotat, France; 30 mm long, 11 mm in diameter) was inserted in the arterial allograft. After bronchial declamping, the proximal anastomosis was completed. To avoid stent migration, the distal part of the stent was secured to the bronchial and allograft wall with 2 separate sutures of 3-0 polypropylene (Fig 1B). The replaced bronchial segment was encircled with the intercostal muscle flap and thus isolated from the neighboring pulmonary artery. Two chest tubes were inserted at the end of the procedure.

Postoperative Evaluation
All animals survived the procedure and were examined daily for about 4 weeks after the operation and monthly thereafter. Data were collected on general status, wound status, cardiac frequency, and respiratory status, noted as presence of breath sounds in the left diaphragmatic pulmonary lobe, quality of breath sounds in the right lung, and presence of symptoms such as dyspnea, cough, and increased pulmonary secretions.

Fiberscopic examination was performed under general anesthesia at 1, 3, and 6 months to assess the patency of the airway and to evaluate possible complications as well as whenever respiratory symptoms demonstrated an obstruction of the left bronchial tree.

Removal of the bronchial stent was accomplished under general anesthesia using a rigid bronchoscopic procedure. It was performed only for animals of group 2: 1 at 9 months and 2 at 12 months.

Histologic Evaluation
Sheep were euthanized at regular intervals up to 18 months (Table 1). Explanted bronchial specimens were longitudinally opened and the bronchial stent was removed. After a macroscopic evaluation, specimens were immediately placed in a 10% formaldehyde solution.


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  		Table 1 Bronchial Replacement With Arterial Allografts: Follow-Up, Clinical Complications, and Histologic Examination
 
For each specimen, two longitudinal sections of graft-containing samples were embedded in paraffin. Four-micrometer-thick slices were stained with hematoxylin-eosin-saffron (HES) and orcein for microscopic examination.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Footnotes
 Acknowledgments
 References
 
Clinical Evaluation
The operation was successful in all sheep, with no perioperative deaths. All animals recovered spontaneous ventilation at the end of the procedure. Thoracic drainage was kept in place for 24 hours. Two sheep required a drain for 48 hours because leaks were present.

In the early postoperative period animals were in good health status and ate normally. Atelectasis was the only early postoperative complication (n = 2; Table 1). This was successfully treated by fiberscopic aspiration of white abundant secretions that accumulated distal to the endoprosthesis.

The late postoperative period was uneventful in 12 sheep, and 13 animals were euthanized as scheduled. Clinical complications occurred in 3 sheep, comprising 1 pulmonary abscess, 1 bronchopneumonia, and 1 atelectasis of the left diaphragmatic lobe due to distortion of the bronchial endoprosthesis (Table 1). A pulmonary abscess developed at 3 months after the bronchial replacement in a group 1 sheep caused by the formation of an obstructive granuloma. Urgent euthanasia was performed in this sheep. Bronchopneumonia occurred at 2 months in a group 2 sheep, which was also urgently euthanized. Stent distortion was revealed at fiberscopic examination in 1 group 2 sheep that presented with alteration of health status at 2 months. The endoprosthesis was removed because it completely obstructed the airflow. During the procedure, fiberscopic control did not show any collapse at the grafted area. This sheep was euthanized at 6 months, as scheduled. The postmortem examination showed a stenosis in the grafted area of about 70% in diameter.

Regular bronchoscopic examination revealed bronchial granuloma formation at 1 month in 3 sheep and mucosal hyperplasia at 3 months in 1. The bronchial stent was removed at 9 months in 1 animal and at 12 months in 2 animals. This did not lead to any complication, neither perioperatively nor afterwards.

Clinical evaluation did not reveal any bronchial stent migration or bronchopleural or bronchovascular fistula.

Macroscopic Findings
Macroscopic examination of bronchial specimens showed a perfect continuity between the grafted area and the adjacent bronchus. A dense, fibrous tissue, less rigid than the bronchial wall, replaced the arterial allograft. A macroscopic phenomenon of contraction of this tissue was observed (Table 1). Contraction was proportional to the age of the specimen. At 6 months, this tissue measured approximately 5 mm in length (Fig 2A). Starting at 12 months, normal proximal and distal bronchial structures were separated by only a thin line of fibrous tissue (Fig 2B). This pathologic finding was independent of the type of arterial allograft used (fresh or cryopreserved).


Figure 2
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  		Fig 2. Macroscopic views of bronchial replacement show longitudinal views of specimens at (A) at 6 months and (B) 12 months.

 
There was no anastomotic fistula, allograft rupture, or bronchovascular fistula.

The group 2 animals that underwent endoprosthesis removal were monitored for another 3 months (n = 1) and 6 months (n = 2). Bronchial specimens showed patency of the grafted area. As previously described, 1 animal in group 2 needed stent ablation at 2 months. This allowed us to study the transformation that occurred with early stent removal. The fibrous tissue retracted towards the bronchial lumen and created a significant stenosis of about 70%.

As mentioned, three cases of granuloma formation were confirmed by the macroscopic examination of specimens. Granuloma was responsible for airway stenosis in 2 sheep and for complete obstruction of the airway with the development of a pulmonary abscess in 1. In 1 sheep, granuloma formation was due to an inhaled foreign body. Intercostal muscle flap presented ossification in all specimens (Fig 2A) and covered circumferentially the bronchial replacement area.

Microscopic Findings
Within the bronchial graft, histologic transformations evolved identically for fresh and cryopreserved arterial allografts. Arterial tissue disappeared, with only remnants of elastic fibers still present in all specimens. A fibrous, solid, healing connective tissue replaced the arterial structure. Normal bronchial tissue with cartilage and glands was present at the extremities. In specimens at 2 months, there was an important infiltration with inflammatory cells towards the luminal part of the healing connective tissue (Fig 3A). At up to 6 months, this inflammatory reaction reduced in intensity proportional to the age of the specimen. After 6 months, a modest inflammatory infiltrate persisted in the connective tissue below the epithelium (Fig 3B).


Figure 3
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  		Fig 3. Microscopic examination of bronchial replacement (hematoxylin and eosin stain) shows (A) squamous epithelium in a 2-month specimen (original magnification x100); (B) respiratory epithelium with cilia (arrow) in a 6-month specimen (original magnification x200); (C) islands of new cartilage in a 6-month specimen (original magnification x 50); (D) islands of immature cartilage (*) in a 2-month specimen (original magnification x 50); (E) bud-like appearance of cartilage island at the edge of the grafted area in a 2-month specimen (original magnification x 200); and (F) islands of new cartilage in a 6-month specimen (original magnification x50).

 
All bronchial specimens presented with progressive surface epithelialization. At the 2-month interval, nonkeratinized squamous epithelium covered the edges of the grafted area (Fig 3A). The center of the graft was not reepithelialized. Epithelium grew from the extremities to cover the entire graft. Thus, at 4 months squamous epithelium was continuous, with respiratory epithelium at the edges. Starting from 6 months, respiratory epithelium progressively predominated (Fig 3B). Some squamous epithelial islands persisted, even in long-term specimens, when the endoprosthesis was still in place when euthanasia occurred. A continuous respiratory epithelium with cilia was seen only in animals in which the bronchial stent had been removed.

The length of the healing tissue actively diminished over time. After 2 months, islands of immature cartilage were visible, mainly at the extremities (Fig 3C and D). Progressively in late specimens, only a thin strap of fibrous connective tissue separated the two normal bronchial ends. Many cartilage islands at the edges consistently showed modified architecture, and they looked longer, with bud-like adjacent islands (Fig 3E and F).

Bone tissue was present at the exterior of the grafted area in an almost circumferential manner. It originated in the periosteum harvested with the intercostal muscle flap.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Footnotes
 Acknowledgments
 References
 
The results of the present study showed that bronchial regeneration is obtained after replacement with an arterial allograft supported by a silicone endoprosthesis. Despite its apparent simplicity, the replacement of the airway was a real challenge for researchers for more than half a century and was marked by numerous complications [14]. Our previous experiments showed that tracheal and carinal replacement with an aortic segment, either an autologous or a fresh allogenic graft, permitted airway regeneration in sheep [9–12]. We recently investigated the use of a cryopreserved aortic allograft for tracheal replacement with the same results [13]. In addition to the achievement of a new tracheal segment, complications were rare and mainly related to mobilization of the tracheal stent. Our results were also confirmed in a pig model [15, 16], and the first clinical applications of tracheal replacement with allogenic aorta have already taken place [17, 18]. Therefore, we considered it adequate to evaluate the same type of substitute for bronchial replacement.

In this study we favored the use of cryopreserved allografts with a view to future clinical applications. Indeed, cryopreserved arterial allografts are presently kept in tissue banks and are available for programmed surgical interventions.

Macroscopically, the grafted area keeps its tubular structure, which progressively rigidifies. Epithelialization was complete after 4 months of follow-up, and scar tissue diminished in length over time. Bronchial tissue, including cartilage, formed within the graft so that only a thin line of scar tissue separated 2 normal bronchial ends at 12 months. At this stage, the macroscopic aspect was the same as if only a bronchial sleeve resection had been performed. This is particularly important because it allows removal of the bronchial endoprosthesis.

Epithelialization of the grafted area advances from the edges, as was previously shown for the trachea and carina [10–12]. A squamous epithelium initially develops that is progressively replaced by a respiratory epithelium. Foci of squamous metaplasia persist even at the 12-month interval and are probably related to the presence of the bronchial stent. As for the trachea and carina, the phenomenon of cartilage regeneration was also observed for the bronchus. Cartilage regeneration, together with the progressive reduction in length of the scar tissue, led to a cartilage rigidified tubular new bronchus. There is growing evidence of the involvement of stem cells in the process of airway regeneration, either local [19, 20] or derived from the bone marrow [21]. We hypothesize that the arterial allograft offers a solid and suitable scaffold for these regenerative processes to take place. Major studies are presently in progress in our laboratory (Laboratoire de Recherches Biochirurgicales, Fondation Alain Carpentier EA, Assistance Publique-Hôpitaux de Paris) to assess the participation of stem cells in the regeneration of the airways after replacement with arterial grafts.

Technically, bronchial replacement was performed safely, without any intraoperative incidents. There were no perioperative deaths, and early postoperative complications were minor: atelectasis of the left diaphragmatic lobe rapidly resolved with fiberscopic aspiration.

One purpose of our study was to identify the possible late complications of the procedure. It is important to note that there were no bronchopleural or bronchovascular fistulas, which are particularly encountered after bronchial sleeve resections [22]. The avoidance of these complications was probably due to the use of the intercostal muscle flap as a source of neovascularization and mechanical protection of the grafted area.

The postoperative course was uneventful in most of the sheep, and the observed complications were related to the bronchial endoprosthesis, including formation of a pulmonary abscess due to an obstructive granuloma, development of bronchopneumonia as secretions accumulated distal to the stent, and late atelectasis due to stent distortion. Mechanical irritation of the mucosa by the bronchial stent was responsible for granuloma formation in 2 sheep. In clinical practice, these complications would have been easily managed or prevented by bronchoscopic granuloma resection, fiberscopic aspiration, stent replacement, and antibiotic treatment.

The endobronchial stent is indispensable because it maintains the rigidity of the graft. Premature stent removal in 1 animal, as a consequence of stent distortion, led to the development of a 70% stenosis of the grafted area. No stenosis occurred when stent ablation was conducted between 9 and 12 months from the bronchial replacement. This was probably due to the progression of the histologic transformation of the grafted area, which became rigidified with cartilage. In human clinical practice, early stent removal would have been avoided, because stent replacement is commonly available.

In human practice, a bronchial substitute would be valuable tool for certain situations of surgical pulmonary resection. Although indispensable for the management of non-small cell lung cancer, resection procedures are source of important perioperative and long-term complications. Thus, pneumonectomy is considered a high-risk procedure for postoperative mortality and long-term alteration of respiratory and cardiovascular function [23, 24]. Current expert opinion is that this operation should be avoided whenever possible in case of induction therapy [25], because unacceptable mortality rates of 21% to 26% have been reported [3, 4, 26, 27].

To avoid the complications of pneumonectomy, sleeve lobectomy has emerged as the preferred operation in case of central non-small cell lung cancer [25] because it has the advantage of preserving the pulmonary parenchyma. However, there are still controversies about whether to consider sleeve lobectomy a curative resection technique for non-small cell lung cancer because it is suspected of a higher rate of locoregional recurrence [6]. Sleeve resection has been reported as a safely procedure in patients with induction therapy [28–30].

Sleeve resection is technically not feasible in certain situations, including when there is extensive tumor infiltration of the main or intermediate bronchus or of the pulmonary artery and when the pulmonary fissure is inaccessible because of diseased lymph nodes [31]. In this context, bronchial replacement would find a clinical field of application because it would permit a more anatomic reconstruction of the airway with longer bronchial resections. Sleeve lobectomy would be performed more often, consequently reducing the necessity of pneumonectomy. On the other hand, there would be a lesser risk of recurrence because surgeons could afford resection margins at a greater distance from tumoral infiltration. Thus, the two main complaints of sleeve lobectomy—unfeasibility and recurrence—would diminish considerably. The importance for the clinical practice of bronchial replacement was also recently stated by Sato and colleagues [32], who proposed a substitute issued from tissue engineering.

In our research study, bronchial replacement with arterial allografts was safe and feasible. Late complications in patients would have been fully preventable by the bronchoscopic treatment of granuloma, bronchial stent replacement, and fiberscopic aspiration. The elective use of a bronchial substitute would be a secure adjunct to the surgical arsenal and would contribute to a reduction in the pneumonectomy rate and of local recurrences associated with sleeve bronchial resections.


   Appendix
 
Harvest and Preservation of Arterial Allografts
Arterial allografts that underwent fresh preservation were submerged in a solution that is currently used in human practice (Appendix Table 1) and preserved at 4°C. The mean preservation time was 11.6 days (range, 5 to 21 days).


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  		Appendix Table 1 Preservation Solution for Fresh Arterial Allografts
 
Arterial allografts that underwent cryopreservation were first maintained for 48 to 72 hours at 4°C in Solution for Organ and Tissue Preservation (SCOT; MacoPharma, Mouvaux, France) containing antimicrobial agents (Appendix Table 2). Afterwards, they were cryopreserved under sterile conditions at –150°C in a 4% dimethylsulfoxide solution.


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  		Appendix Table 2 Preservation Solution Used for Allografts That Underwent Cryopreservation
 
Technical Details
Anesthesia induction was achieved using intravenous propofol 1% (6 mg/kg). After endotracheal intubation, anesthesia was maintained with inhaled 60% oxygen and 2.5% to 3% isoflurane. Ventilation was performed with a Siemens 900C ventilator (Siemens Medical Systems, Inc., Iselin, NJ), with tidal volume at 10 mL/kg and 24 breaths/min. When necessary, pulmonary exclusion was obtained by clamping the left main bronchus at its origin. To reduce barotrauma in 1-lung ventilation, ventilation variables were modified, with same minute ventilation, 34 breaths/min, and reduced tidal volume.

Animals were monitored during anesthesia by continuous electrocardiogram, arterial blood pressure, and pulse oximetry. Arterial blood gazes were regularly checked during the procedure.

Animals of group 1 and group 2 were perfused with a crystalloid solution (10 mL/kg/h).

Antibiotic prophylaxis consisted of 1 gram of cefazolin after anesthesia was induced and 1 gram after 4 hours. In the early postoperative period, 1 gram of cefazolin was injected intramuscularly every day for 7 days. No immunosuppressive therapy was given.

Euthanasia was performed by an intravenous injection of thiopental sodium (3 g) and potassium chloride (3 g).


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
References
 
This study was supported by a grant from the Société de Pneumologie de Langue Française. Silicone bronchial stents were kindly provided by Mr. Bruno Ferreyrol (Novatech, La Ciotat, France). We thank Nathalie Goussef, Martine Rancic and Martine Douheret for their technical assistance. We also thank Hamdane Tandjaoui, MD, for the fiberscopic evaluation.


   Footnotes
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
Acknowledgments
 References
 
* Co-directors of the study. Back


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 

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E. Martinod, D. M. Radu, K. Chouahnia, A. Seguin, A. Fialaire-Legendre, P.-Y. Brillet, M.-D. Destable, G. Sebbane, S. Beloucif, D. Valeyre, et al.
Human Transplantation of a Biologic Airway Substitute in Conservative Lung Cancer Surgery
Ann. Thorac. Surg., March 1, 2011; 91(3): 837 - 842.
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