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Ann Thorac Surg 2008;86:422-428. doi:10.1016/j.athoracsur.2008.04.015
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Replacement of the Left Main Bronchus With a Tissue-Engineered Prosthesis in a Canine Model

Toshihiko Sato, MDa,*, Hiroyuki Tao, MDb, Masato Araki, MDc, Hiroki Ueda, PhDd, Koichi Omori, MDe, Tatsuo Nakamura, MDa

a Department of Bioartificial Organs, Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan
d Department of Biomaterials, Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan
b Department of Thoracic Surgery, Okayama University, Okayama, Japan
c Division of Surgical Oncology, Department of Translational Medical Sciences, Nagasaki University, Nagasaki, Japan
e Department of Otolaryngology, Fukushima Medical University, Fukushima, Japan

Accepted for publication April 3, 2008.

* Address correspondence to Dr Sato, Department of Bioartificial Organ, Institute for Frontier Medical Sciences, Kyoto University, 54 Kawaharacho Shogoin Sakyoku, Kyoto, 606-8507, Japan (Email: tsato{at}frontier.kyoto-u.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Stenosis of the left main bronchus caused by inflammatory diseases and neoplasms is a serious clinical problem because it can cause obstructive pneumonia and may require pneumonectomy. As an alternative to various treatments currently available, including balloon dilatation, stenting, and bronchoplasty, we propose the use of a prosthesis developed based on the concept of in situ tissue engineering for replacement of the left main bronchus.

Methods: The main frame of the tissue-engineered prosthesis is a polypropylene mesh tube, 12 to 15 mm in inner diameter and 30 mm in length, with reinforcing rings. Collagen extracted from porcine skin is conjugated to this frame. A consecutive series of 8 beagle dogs underwent replacement of the left main bronchus with this tissue-engineered prosthesis.

Results: All dogs survived the postoperative period with no morbidity except 1, which required intravenous administration of antibiotic for a week for pneumonia and recovered. Three dogs were euthanized for examination at 3 and 4 months after bronchus replacement, and the other five were monitored for more than 1 year. In two dogs, histologic examination revealed that the luminal surface was completely covered with ciliated columnar epithelium or nonciliated squamous epithelium. Exposure of the polypropylene mesh to various degrees was observed in 6 dogs, but the prosthesis remained stable and no adverse effects such as infection, sputum retention, or dehiscence were observed.

Conclusions: These long-term results suggest that our tissue-engineered prosthesis is applicable for replacement of the left main bronchus.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Various therapeutic approaches for bronchial stenosis and obstruction have been reported, including bronchoscopic dilatation, laser ablation, airway stenting, and surgical bronchoplasty [1–3]. The objective of the present study was to test a possible alternative for the treatment of bronchial stenosis and obstruction. We have been developing a porous type of airway prosthesis conjugated with a collagen layer based on the concept of in situ tissue engineering. The intent of n situ tissue engineering is to create a local environment with a prepared scaffold suitable for tissue or organ restoration [4]. We have applied a collagen layer as a three-dimensional scaffold, which provides an appropriate environment into which surrounding host cells can migrate and proliferate, and applied it for regeneration of the trachea [5–8], esophagus [9, 10], stomach [11, 12], intestine [13], and peripheral nerves [14–16]. Collagen is a major component of the extracellular matrix and is known to promote cellular proliferation and tissue healing.

With this type of prosthesis, we have previously reported replacement of the intrathoracic trachea [5–7] and carinal part of the trachea [8] in animal experiments and the cervical trachea in humans [17, 18]. On the basis of these experiences, we designed a new prosthesis and adopted it for experimental replacement of the left main bronchus in dogs.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Bronchial Prosthesis
The collagen-conjugated bronchial prosthesis (20 mm long with an internal diameter of 12 to 15 mm) was made by a method similar to that described in our previous report concerning tracheal and carinal reconstruction [5]. The prosthesis consists of a fine polypropylene mesh cylinder with a pore size of 260 µm (Marlex mesh, CR Bard Inc, Billerica, MA), reinforced with 5 rings of polypropylene monofilament string (1 mm in diameter) wrapped around it. These rings were attached to the cylinder by thermal melt bonding to maintain the proper cylindrical form. This mesh cylindrical frame was exposed to a corona discharge at 9 kV for 5 minutes to make its surface hydrophilic.

The prosthesis was placed into a mold. A 2% collagen solution (supplied by Nippon Meat Packers Inc, Osaka, Japan) was poured into the mold, followed by freeze-drying, to form a collagen layer 5 mm thick around the frame. In this process, the collagen became an amorphous layer with a pore size of 100 to 500 µm. The prosthesis was heated at 140°C under vacuum for a single or double 24-hour session of dehydrothermal treatment to induce moderate cross-linkage in the collagen molecules. Finally, the prosthesis was sterilized with ethylene oxide gas and stored dry until use. Figure 1A shows the polypropylene frame, and Figure 1B shows the collagen-conjugated prosthesis, which appears swollen after being soaked in blood.


Figure 1
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  		Fig 1. (A) The bulk structure of the prosthesis consists of a mesh cylinder reinforced with 5 rings of polypropylene string (left) and a covering of conjugated collagen (right). (B) This outer view shows the outer prosthesis conjugated with a collagen layer after it has been soaked with blood, just before replacement.

 
Animal Experiment
Eight adult beagle dogs, weighing 8 kg to 15 kg, were anesthetized by the intramuscular administration of ketamine hydrochloride (15 mg/kg) and xylazine (7 mg/kg) and then intubated with an endotracheal tube. Respiration was maintained by a mechanical ventilator with halothane and nitrous oxide gas. A left thoracotomy was made through the 4th or 5th intercostal space according to the physique of each dog. The left main bronchus was exposed from the spur of the left upper bronchus to the carinal edge through the pulmonary aorta window. After the main bronchus had been transected at the spur of the left upper bronchus, the distal end was anastomosed with interrupted 3-0 Vicryl suture (Ethicon Inc, Somerville, NJ) to the prosthesis (Fig 2), which had been previously soaked with blood.


Figure 2
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  		Fig 2. (Top) This drawing shows the schematics of the bronchial reconstruction. (Bottom) This photograph was taken during bronchial replacement with the artificial prosthesis (arrowhead). (Ao = aorta; PA = pulmonary artery.)

 
A 10-mm segment of the left main bronchus was resected and the carinal stump was anastomosed to the proximal end of the prosthesis. Both ends of the prosthesis were intended to be anastomosed in a telescopic manner, the bronchial end lying inside the prosthesis. A pedicled pericardial fat pad was fixed to the surrounding structure to cover the prosthesis.

The dogs were appropriately hydrated with extracellular fluid, and hydrocortisone (125 mg) was administered during the operation. Ampicillin was given intravenously at a dose of 1 g on the day of the operation and at 0.5 g daily for 3 days thereafter. Hydrocortisone (125 mg) was administered intravenously for 3 days after the procedure. All the animals received humane 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.)

Bronchoscopic Observation
Bronchoscopic observation was done periodically after induction of general anesthesia by an intramuscular injection of ketamine hydrochloride and xylazine hydrochloride. The luminal surface was observed with a bronchofiberscope (Model BF1T20, Olympus Optical Company, Ltd, Tokyo, Japan) to evaluate the coverage by host tissue and complications such as stenosis and dislocation of the prosthesis (Fig 3).


Figure 3
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  		Fig 3. (A) Bronchoscopic views of dog 8 taken 18 months after tracheal replacement. Neither stenosis nor granulation is evident at the site of anastomosis. Black arrow shows the carina. The prosthesis was fully covered with regenerated tissue. (B) White arrows show the regenerated portion of the bronchus.

 
Evaluation of the Prosthesis
The replaced portion was examined bronchoscopically and macroscopically (Fig 4) after necropsy. Mesh exposure exceeding one-third of the circumference was defined as "exposed," and less than one-third as "spot exposed." Stenosis was defined as a reduction of more than one-third of the tracheal lumen cross-sectional area. Euthanasia was performed by intravenous injection of ketamine hydrochloride at a dose of 100 mg/kg, followed by necropsy.


Figure 4
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  		Fig 4. Macroscopic view shows of the luminal surface of the prosthesis of dog 8 at 18 months after replacement. Arrows show the regenerated part. The luminal surface is covered with apparently normal mucosa, which is continuous with the native bronchus and appears whitish.

 
Histologic Examination
Immediately after macroscopic evaluation, specimens were placed in 10% formaldehyde solution, followed by paraffin embedding. Sections 5 µm thick were stained with hematoxylin and eosin for light microscopy. Another part of each fresh specimen was fixed with 2% glutaraldehyde and critical-point-dried by Au-Pd sputtering for scanning electron microscopic examination.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
The outcome of the experiments is reported in Table 1. All the dogs survived postoperative period without measurable morbidity, but severe pneumonia developed in 1 dog. Bronchoscopic and radiologic findings showed that this pneumonia was caused by postoperative atelectasis. This dog (No. 1 Table 1) recovered after the intravenous administration of antibiotic for a week and showed no dehiscence of anastomosis, or infection to the prosthesis during postoperative period.


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  		Table 1 Results of Replacement of the Left Main Bronchus
 
Bronchoscopic and Macroscopic Examination
Stenosis and excessive granulation were observed in dogs 2 and 3. One possible reason for the stenosis might have been mismatching of the prosthesis size in these 2 dogs, the prosthesis diameters being 12 and 13 mm, respectively, which were considered too small for the purpose. No stenosis or excessive granulation developed in the other 5 dogs, whose left main bronchi were replaced with a 15-mm-diameter prosthesis. Thus, the stenosis might have been caused by the small size of the prosthesis.

The evaluation for mesh exposure showed 4 dogs were classified as "exposed," 2 as "spot exposed," and 2 as fully covered. Dogs 2 and 3, which developed excessive granulation and stenosis, also showed concomitant mesh exposure.

Because mesh exposure was prominent in the first 4 dogs in this series, we reduced the dehydrothermal treatment time to 24 hours, with the expectation that this would enhance cell immigration to the prosthesis wall in the last 3 dogs. Complete epithelization was achieved in 2 dogs of this group, but the epithelization remained partial in 1 dog.

The host tissue incorporated into the framework of the prosthesis, and neither erosion nor nonfavorable interaction was observed between the framework and the adjacent vessels. No complications such as hemoptysis or intrathoracic hemorrhage were observed.

Histologic Findings
Ciliated columnar epithelium was microscopically observed near the anastomosis, but the proportion of squamous epithelium became larger than that of ciliated columnar epithelium with increasing distance; near the center of the prosthesis, only squamous epithelium was recognized (Fig 5, Fig 6). No immigration of inflammatory cells under the regenerated epithelium was evident, indicating that the prosthesis was well incorporated without an excessive foreign body reaction, which may lead to formation of granulation tissue and stenosis.


Figure 5
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  		Fig 5. Microscopic examination of a longitudinal section of the regenerated tissue 18 months after replacement (hematoxylin and eosin staining). (A) Regenerated neomucosa with epithelial lining is observed on the prosthesis. (B) Ciliated epithelial cells have grown over the prosthesis showing continuity with the native bronchial epithelia, whereas (C) the center of the prosthesis is covered with a monolayer of squamous epithelium. (L = bronchial lumen, P = polypropylene mesh.) (Original magnification: x10 for A, x40 for B, x100 for C.)

 

Figure 6
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  		Fig 6. Scanning electron microscopy findings of the prosthesis 18 months after replacement. (A) The proximal portion of the anastomosis is covered with ciliated epithelial cells (x2500; bar, 20 µm), whereas (B) fewer such cells are observed in the middle of the prosthesis (x1000; bar, 50 µm).

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Reconstruction of the airway with an artificial prosthesis has been studied for decades. However, the degree of success has been limited because of problems such as local infection, stenosis, or rupture of the adjacent vessels [19–21]. The risk of such fatal complications currently precludes the clinical use of artificial prostheses in this situation.

Most recently, tissue-engineering techniques have been applied to regenerate a biologic prosthesis for implantation. Using ex vivo tissue engineering techniques, Kojima and colleagues [22] successfully created a tissue-engineered trachea with regenerated cartilage from bone marrow cells. However, the transplantation of such ex vivo tissue-engineered tissues has been associated with poor functional outcome [23, 24], and so their application is still problematic.

Another biologic approach for creation of prostheses has been reported by Martinod and colleagues [25]. They applied allogenic aorta for tracheal replacement, and the transplant was proven to be functional after removal of the inner stent [25, 26]. It is noteworthy that the allotransplant was replaced by a completely regenerated trachea provided with cartilage rings derived from the recipient. There is a similarity between their approach and ours, because the basic idea of in situ tissue engineering is to produce an environment suitable for host tissue regeneration at the required site.

The aortic graft played the role of a biologic incubator to allow host cells to migrate into it and form the regenerated trachea. One dissimilarity was that we used a polypropylene permanent framework as a substitute for cartilage, whereas they applied an internal stent temporarily. Wurts and colleagues [27] have reported clinical application of this type of approach, and we await their long-term results, which may indicate whether cartilage would be generated in adult humans.

The requirements for an ideal prosthesis are (1) adequate durability that can be maintained long enough to restore the functional airway, (2) high biocompatibility, enabling incorporation into the host tissue, and (3) relatively low cost. We have been investigating a tissue-engineered collagen-conjugated prosthesis that potentially meets these requirements. Okumura and colleagues [5] designed a tracheal prosthesis consisting of a rigid polypropylene frame and a collagen monolayer. Animal experiments showed that this type of prosthesis has high biocompatibility with host tissue and overcomes serious major complications such as anastomotic leakage or postanastomotic stenosis. [7] With regard to mechanical properties, this type of tissue-engineered tracheal prosthesis has appropriate mechanical properties similar to those of the native trachea [28], and its feasibility has been proven by observation for more than 5 years in a canine tracheal replacement model [29]. For the cervical trachea, Omori and colleagues [17, 18; unpublished data] have applied this tissue-engineered tracheal prosthesis for 8 patients to date, with a maximum follow-up period of 4 years.

In terms of biocompatibility, we have developed a prosthesis conjugated with a thick collagen layer after a trial with a collagen monolayer type. Using this type of prosthesis, Teramachi and colleagues [6, 7] have achieved intrathoracic tracheal replacement, and Sekine and colleagues [8] have reported that a Y-shaped prosthesis for carinal reconstruction in a canine model showed good incorporation into the host tissue [6]. We consider that the collagen layer, which has a three-dimensional structure and provides an appropriate extracellular matrix in which migrating cells can proliferate, potentially enhances tissue regeneration.

As for affordability, this type of prosthesis is suitable for commercial production in various sizes and lengths at a low cost compared with biologic transplants and is free from any risk of donor infection. We used ethylene oxide gas for sterilization, because gamma-ray irradiation may have a degradative effect on collagen fibers. Gorham and colleagues [30] reported that neither method of sterilization of collagen-based wound repair materials produced any cytotoxic effect, although gamma-ray sterilization, which is more convenient, did lead to accelerated absorption.

On the basis of our previous experiences, we designed a prosthesis for replacement of smaller portions of the airway and applied it for repair of left main bronchial defects in a canine model. The aim of the present study was to clarify whether our previously developed tissue-engineered prosthesis would be applicable for smaller airway defects and to determine the optimum conditions for its use.

Severe stenosis developed in 2 of 3 dogs in which the left main bronchus was replaced with a 12-mm-diameter prosthesis. In contrast, no stenosis developed in the 5 dogs in which the bronchus was replaced with a 15-mm prosthesis. These results show that the inner diameter of the prosthesis should be 15 mm for replacement of the canine left main bronchus, which has a caliber of 10 to 12 mm, as measured at the site during the operation.

For the preparation of the collagen solution and the conditions for cross-linkage of the collagen molecules, we started with 1% collagen solution and 24 hours of dehydrothermal treatment. However, in the 2 dogs that received this type of prosthesis, the disruption of the prosthesis wall caused tension pneumothorax that proved to be too fragile for sealing the peripheral airway without an inner lining. These initial 2 dogs that were fitted with the 1% collagen prosthesis were therefore eliminated from the study. A prosthesis made with 2% collagen and cross-linked for 48 hours was applied in consecutive experiments, and the wall of this prosthesis proved sufficiently durable to withstand the airway pressure. However, mesh exposure was prominent with this type of prosthesis, and epithelization of the lumen was poor compared with our previous study, in which 90% of dogs showed no mesh exposure.

Unlike our previous procedures for replacement of the intrathoracic trachea and carina [6, 8], we did not insert a silicone tube inside the prosthesis for extraction 8 weeks after implantation. This silicone tube had played a role in protecting the collagen layer from early degradation before tissue formation. However, because the canine left bronchus was considered too small for application of a silicone tube, we intended to try a simpler procedure. To improve epithelization, we reduced the dehydrothermal treatment time. Dehydrothermal treatment for 48 hours gives the collagen layer mechanical strength but may denature the collagen and thus decrease its favorable characteristics. Although we have not performed a sufficient number of trials to obtain precise data, it appears that collagen loses its ability to promote cell proliferation after 48 hours of dehydrothermal treatment because of excessive cross-linkage between the collagen molecules. Prostheses coated with 2% collagen that had been exposed to dehydrothermal treatment for 24 hours were transplanted with the expectation that this reduction in dehydrothermal treatment time would improve tissue regeneration. Two of the three dogs showed complete epithelization and no mesh exposure, and none showed dehiscence, disruption of the prosthesis wall, or stenosis. We therefore concluded that coating with 2% collagen solution and 24 hours of dehydrothermal treatment are the optimum conditions for preparation of the prosthesis.

In this canine model using the left main bronchus, the time for tissue regeneration was estimated to be 3 to 4 weeks by bronchoscopic observation. In patients where the cervical trachea was reconstructed, tissue regeneration was considered to take rather longer; Omori and colleagues [18] reported that this period ranged from 2 to 11 months in patients undergoing cervical tracheal replacement. Because no infection or dehiscence before complete epithelization occurred in these patients, mesh exposure might not be a fatal problem. However, to accomplish better epithelization, we are now investigating an improved prosthesis in which the luminal surface is lined with biodegradable polymer. In this new trial, we are observing better epithelization, with 90% of candidates accomplishing complete epithelization, although the observation period is not yet long enough.

We designed a new prosthesis for peripheral airway reconstruction. In a canine left main bronchus replacement model, this collagen-conjugated polypropylene prosthesis showed sufficient mechanical strength to support the airway without causing stenosis, and good biocompatibility. Although further assessment is essential before clinical application, our designed prosthesis may be a promising alternative for the treatment of left main bronchial stenosis and obstruction.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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