Ann Thorac Surg 1998;66:1777-1781
© 1998 The Society of Thoracic Surgeons
Original articles: general thoracic
Experimental study of tracheal patch reconstruction with a covered expandable metallic stent
Hidehiko Kitagami, MDa,
Toshiyuki Takahashi, MD, PhDa,
Satoshi Watanabe, MD, PhDb,
On Suzuki, MDa,
Toshiaki Morikawa, MDa,
Shun-ichi Okushiba, MD, PhDa,
Hiroyuki Katoh, MD, PhDa
a Second Department of Surgery, Hokkaido University School of Medicine, Sapporo, Japan
b Third Department of Anatomy, Hokkaido University School of Medicine, Sapporo, Japan
Accepted for publication May 17, 1998.
Address reprint requests to Dr Takahashi, Second Department of Surgery, Hokkaido University School of Medicine, N-14, W-5, Kita-ku, Sapporo 060-8638, Japan
e-mail: (ricoh{at}med.hokudai.ac.jp)
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Abstract
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Background. We evaluated the efficacy of tracheal patch reconstruction with a covered expandable metallic stent (EMS) with omentoplasty.
Methods. After resecting the right half of the circumferential wall of two tracheal rings in adult beagle dogs, we inserted a covered EMS to reconstruct the defect interiorly. Then, through laparotomy, we made an omental pedicle flap and wrapped it around the EMS-interposed area. For comparison with the group without omentoplasty, we periodically examined the healing process macroscopically and histologically.
Results. Bronchofiberscopic observations revealed that incorporation of the covered EMS progressed with the passage of time and tracheal luminal patency was maintained well in both groups. However, polyplike granulation developed gradually at both ends of the EMS. Histologically, epithelium was regenerated in the patched area 4 weeks postoperatively and the area was covered with pseudostratified ciliated epithelium at 12 weeks postoperatively. Quantitative analysis of the macroscopic and histologic findings showed that the inflammatory polyps were reduced and epithelialization was promoted in the group with omentoplasty.
Conclusions. Tracheal patch reconstruction with a covered EMS, when combined with omentoplasty, promoted early epithelial regeneration and suppressed the development of inflammatory polyps.
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Introduction
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Along with advances in surgical techniques to deal with malignant thoracic tumors, situations requiring reconstruction of the trachea are increasing. Although partial tracheotomy is considered clinically effective as it resects only the tumor-invaded area, it is not yet established as a manageable operation because no decisive patch material that fulfills the criteria of flexibility, sputum secretion, and luminal patency is available. Noting that the covered expandable metallic stent (C-EMS) may fulfill the three requirements for the material and that its installation is fairly easy, we attempted to apply the C-EMS to tracheal patch reconstruction. In this study, we made a model for the reconstruction of a tracheal defect using the C-EMS and evaluated the usefulness of the material and the efficacy of omentoplasty for the healing process.
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Material and methods
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Preparation of C-EMS
The EMS (Z stent) was made of 0.45-mm-diameter stainless-steel wire with a 15-mm luminal diameter and a 25-mm length and with six bends. The covering of the EMS was made of polyglycolic acid (PGA) mesh (0.18 mm thick, 0.25 mm pore size). Two thirds of the EMS circumference was covered with PGA mesh, which was fixed to the EMS with 7.0 nylon thread at the four corners (Fig 1A).
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Fig 1. (A) Covered expandable metallic stent (C-EMS). (B) Operative method. The right circumferential half of two tracheal rings of the cervical trachea is resected and the C-EMS is interposed in the defect.
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Surgical manipulation
A total of 25 adult beagle dogs (male and female) weighing 8 to 10 kg were used. They were divided into group A (n = 13) and group B (n = 12). Animal care complied with the Guide for the Care and Use of Laboratory Animals, Hokkaido University School of Medicine (HUSM publication, 1988). The dogs were anesthetized with intravenous administration of pentobarbital sodium (25 mg/kg) and were intubated and mechanically ventilated in room air. They were operated on as follows.
Group A
The neck was vertically incised and the peritracheal sheath of the four tracheal rings was freed. The right half of the circumferential wall of the trachea in two of the four freed tracheal rings was resected. A C-EMS was interposed through the defect of the tracheal wall with forceps and the stent cover was matched to the defect (Fig 1B). Through a transverse incision in the upper abdomen, we made an omental pedicle flap with the right gastroepiploic artery as the pedicle to lift it to the cervix through a subcutaneous tunnel in the anteriothorax and wrap around the reconstructed area.
Group B
The operation was carried out as in group A except for omentoplasty.
The tracheal wall excised at operation was fixed in phosphate-buffered 10% formalin as a normal tracheal specimen for histologic studies. Cephalosporin antibiotics were administered intravenously to the dogs for 2 days after the operation.
Evaluation
Bronchofiberoscopy
The lumen of the trachea was examined using bronchofiberoscopy immediately after operation, at 1 week and 3 weeks postoperation and every 3 weeks thereafter.
Macroscopic examination
The dogs were killed by rapidly infusing KCl intravenously at 4 (group A, n = 7; group B, n = 6) and 12 weeks postoperation (group A, n = 6; group B, n = 6) and the reconstructed trachea was resected. The tracheal segment was cut vertically at the cartilages of the unpatched area and opened. Immediately after macroscopic examination of the inner surface, the segment was fixed in phosphate-buffered 10% formalin for 24 hours.
Macroscopic findings were fed into a computer (Power Macintosh Apple Cupertino, CA) for image analysis by an image analyzer (NIH image program). Round protuberances that had grown higher than 2 mm at the C-EMS–interposed area were counted as polyps. The area ratio of the polyps was calculated as follows: Ratio (%) = (Polyp occupying area/C-EMS–interposed area) x 100.
Histologic examination
After formalin fixation, the entire tracheal segment was sectioned lengthwise at 4-mm intervals to obtain longitudinal strips of specimens. The strips were embedded in paraffin and 3-µm-thick serial sections were made from each strip. The sections were then stained with hematoxylin and eosin and examined under a light microscope. The microscopic images of the sections were fed into the computer for measurement of the epithelial length by the image analyzer. The data obtained above were processed to construct a two-dimensional map of epithelial distribution. Then, epithelia-regenerated areas in the patched area were measured from the map to calculate the ratio of regenerated epithelium to the entire patched area. The counts of blood vessels and the areas they occupied in the regenerated submucosal tissue were done by the line-sampling method [1] per ten fields (0.12 mm2/field) at x400 magnification. On this basis, the numbers of blood vessels per square millimeter and their area ratios (percent) per square millimeter were calculated. The same calculation was carried out for the normal tracheal section resected at operation.
All values of macroscopic and microscopic examinations were expressed as mean ± standard error and statistically analyzed by the Mann–Whitney test. Values of p less than 0.05 were considered significant.
Observation of omental pedicle flap artery
To confirm the vascular intercourse of the omental flap with the trachea, at 4 weeks postoperatively, we killed some of the dogs in group A and performed laparotomy. Then, 30 mL of gelatinized blue ink (37°C) was infused at 150 mm Hg into the right gastric omental artery after perfusion of 30 mL of heparinized physiologic saline solution. Then the trachea was resected for macroscopic and microscopic examinations as previously described.
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Results
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None of the dogs had air leakage in both groups throughout the observation period. An airtight seal was created even in group B without omentoplasty because pores of PGA mesh were small enough to be easily stuffed with exudate and it was covered with the muscle surrounding the trachea. Of a total of 25 dogs, 1 in group B died from tracheal occlusion caused by exuberant granulation at 6 weeks postoperatively, and 1 in group A died from collapse of the EMS.
Bronchofiberscope
In both groups, patency of the trachea and fixability of the EMS were satisfactory immediately after operation and thereafter. At 3 weeks after the operation, the stent wire had started to be incorporated in the patched area in both groups. At 6 weeks after the operation, the stent wire was only partially traceable in the lumen and PGA mesh was not recognizable. Small edematous protuberancies were observed where the EMS ends were incorporated. At 9 and 12 weeks postoperatively, polyplike granulations were observed at the EMS ends.
Macroscopic examination
In both groups granulation developed in the patched area and the EMS was incorporated in the granulation tissue at 4 weeks postoperatively (Figs 2A, 2B). Polyglycolic acid mesh was not recognizable. In the unpatched area, the epithelium was pressed by the expanding force of the EMS, which was, however, not incorporated (Figs 2A, 2B). At 12 weeks postoperation the EMS was incorporated circumferentially and was covered with a thin lustrous tunica in both groups (Figs 2C, 2D). Polyps were found in both groups (Figs 2C, 2D), particularly at both ends of the C-EMS in group B (Fig 2D). The counts of polyps and their occupying area ratio were significantly higher in group B than in group A (Table 1).
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Fig 2. Macroscopic findings of the inner surface of the trachea and histologic distribution of the patched area. (A) Group A at 4 weeks postoperatively. (B) Group B at 4 weeks postoperatively. (C) Group A at 12 weeks postoperatively. (D) Group B at 12 weeks postoperatively. In the photograph showing the findings of the resected trachea, the head side is placed on the right and the patched area is enclosed in black squares. Polyps are seen at 12 weeks postoperatively, particularly at both ends of the covered expandable metallic stent in group B (arrows). (Black area = pseudostratified ciliated epithelium; dotted area = pseudostratified columner epithelium; lined area = Stratified squamous epithelium; white area = no epithelium.)
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Histologic examination
At 4 weeks postoperatively, the histologic view in the patched area was in the order: pseudostratified ciliated epithelium, pseudostratified columnar epithelium, and stratified squamous epithelium from the periphery toward the center in both groups (Figs 2A, 2B), but no epithelium was observed in the middle of the patched area in either group (Figs 2A, 2B). Regenerated submucosal tissue was edematous and infiltrated by neutrophils and lymphocytes. In both groups, the epithelium in the unpatched area was pseudostratified ciliated epithelium. Tracheal glands were observed only in the unpatched area. At 12 weeks postoperation the patched area was mostly covered with pseudostratified ciliated epithelium in both groups (Figs 2C, 2D).
Quantitative analysis of histologic findings revealed that ciliated epithelium was larger and the no-epithelium area was smaller in group A than in group B at 4 weeks postoperation (Table 2). At 12 weeks after the operation, no significant difference was observed between groups (Table 2). The counts of blood vessels in the regenerated submucosal tissue increased at 4 weeks postoperatively and decreased at 12 weeks postoperatively in both groups compared with those in the normal submucosal tissue (Table 3). Group A at 4 weeks postoperatively had a significantly large number of blood vessels (Table 3). The area ratio of the blood vessels was high in both groups at 4 weeks postoperatively compared with that in the normal submucosal tissue. At 12 weeks postoperatively the ratio was lower in group A, whereas it was even higher in group B, compared with those at 4 weeks postoperatively (Table 3).
Observation by staining omental pedicle flap artery
Blue stain was macroscopically observed in the lumen of the resected trachea segment. Histologically, the stain was also recognized in the submucosal blood vessels in the unpatched area and the patched area alike.
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Comment
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The tracheal patch materials thus far reported are either autologous, such as pericardium, skin, periosteum, and pedicled muscle flap [2–4], or prostheses such as Marlex (Davol, Cranston, RI) mesh, artificial blood vessels, and absorbant mesh [5–7]. Although further improvements have been made to these, tracheal patch reconstruction is not yet a decisive method because of its complexity and resultant complications.
The EMS has been noted to be effective for stenotic lesions of blood vessels, the bile duct, the trachea, and the bronchus since Wright and associates [8] introduced the Z stent in 1985. However, stability, tissue affinity, and patency of the lumen are not yet satisfactory and its application to the trachea requires considerable improvements. On the other hand, the omentum teems with flows of lymph and blood and has vital angiogenicity as well as a strong antiinflammatory effect [9, 10]. It was also reported recently that omentum is effective for neovascularization in the ischemic tissue of transplanted tracheal sections and in artificial material [11–13]. In this study, we attempted to develop a method of tracheal patch reconstruction, noting the advantages of the supportability and elasticity of the EMS, and examined whether the healing process in the patched area could be promoted by wrapping it in an omental pedicle flap.
It is generally known that when defects occur in the normal trachea, regeneration of the tracheal epithelium is initiated first by covering the defect with squamous epithelium, which is then replaced by ciliated epithelium with the passage of time [14]. Although this experimental model was applied for such a short tracheal defect of two rings, we confirmed the transition process from squamous to ciliated epithelium in the patched area by periodical histologic examination. In this investigation, the patched area—even its middle part—was mostly covered with pseudostratified ciliated epithelium in both groups at 12 weeks postoperatively. Thus, we presumed the epithelialization had finished within 12 weeks in the short tracheal defect as well as this experimental model. In the near future, we hope to examine how healing will proceed for longer defects in another experiment of tracheal reconstruction.
Comparison of the area ratios of the regenerated epithelia between the groups revealed that postoperatively, early epithelialization was promoted by omentoplasty. Other reports indicate that the omentum used for wrapping the tracheal reconstruction provides epithelial regenerating sites with early blood supply [11, 15]. As a result of evaluation of the angiogenic effects of the omentum in the patched area, we found that the granulation healed nearly to the normal level in the group with omentoplasty. This finding appeared to indicate that the angiogenic peak of the granulation was earlier with omentoplasty and that a sufficient blood supply was available to the granulation. Consequently, healing of the granulation, the basis for epithelialization, was promoted and resulted in the completion of satisfactory epithelialization.
Development of inflammatory polyps was markedly suppressed in the unpatched area as well as in the patched area by omentoplasty. It was reported earlier that with omentoplasty native blood vessels at the anastomosis of the trachea have vascular intercourse with the omentum and a good blood supply is obtained from the omentum, which promotes healing [13, 16]. Another report stated that omentoplasty is effective in suppressing the development of inflammatory cells and alleviating inflammatory responses [17]. We presume that the omentum introduced new lymphatic and venous channels into the patched area as shown by microscopic examination in this experiment, resulting in suppression of the development of inflammatory polyps by its antiinflammatory function.
Our work revealed that regeneration of the tracheal epithelium was promoted and development of inflammatory polyps was suppressed by omentoplasty in tracheal patch reconstruction with a covered EMS. The nonelasticity in the longitudinal diameter of the stent may be a problem for patch reconstruction of the trachea. Since Wright and colleagues first [8] introduced the Z stent, several kinds of mesh wire stents, including the Wallstent (Schneider, Bulach, Switzerland) [18] and the Ultraflex (Boston Scientific, St Albans, UK) stent [18], have been constructed and now clinically applied. Use of these stents in our study might lead to better results. Regrettably, there are reports of possible accidents owing to EMS collapse or tracheal perforation in the use of currently available metallic stents, imposing problems with long-term use of the EMS [19, 20]. We emphasize that the metallic stent, which is clinically applied today, is not ideal in permanency and should be used only in people with malignancy and a limited life span. This method will be actually applicable when an advanced type of stent with good mobility and made of a highly absorbent material becomes available.
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References
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|---|
- Weibel E.R. Sampling of tissue. In: Weibel E.R., ed. . Stereological methods. London: Academic Press, 1979:63-100.
- Smolle-Juettner F., Pinter H., Pongtratz G., Ratzenhofer B., Popper H., Friehs G. Closure of bronchial defects using a pedicled pericardial flap. Ann Thorac Surg 1993;56:923-926.[Abstract]
- Cohen R.C., Filler R.M., Konuma K., Bahoric A., Kent G., Smith C. A new model of tracheal stenosis and its repair with free periosteal grafts. J Thorac Cardiovasc Surg 1986;92:296-304.[Abstract]
- De Mello-Filho F.V., Mameda R.C.M., Sader A.A., Velludo M.A.S.L., Vicente W.V.A. Use of the platysma myocutaneous flap for cervical trachea reconstruction: an experimental study in dogs. Laryngoscope 1993;103:1161-1167.[Medline]
- Yamato Y. Experimental study of patch reconstruction of tracheal defects with Marlex mesh. J Jpn Assoc Thorac Surg 1992;40:520-529.
- Shaha A., DiMaio T., Money S., Krespi Y., Jaffe B.M. Prosthetic reconstruction of the trachea. Am J Surg 1988;156:306-309.[Medline]
- Okumura N., Nakamura T., Shimizu Y., Ikada Y., Shiraki K. Study on the repair of tracheal defects using bioabsorbable mesh. Jpn J Artif Organs 1992;21:328-333.
- Wright K.C., Wallace S., Charnsangavej C., Carrasco C.H., Gianturco C. Percutaneous endovascular stents: an experimental evaluation. Radiology 1985;156:69-72.[Abstract/Free Full Text]
- Goldsmith H.S., Griffith A.L., Kupferman A., Catsimpoolas N. Lipid angiogenic factor from omentum. JAMA 1984;252:2034-2036.[Abstract/Free Full Text]
- Cartier R., Brunette I., Hashimoto K., Bourne W.M., Schaff H.V. Angiogenic factor: a possible mechanism for neovascularization produced by omental pedicles. J Thorac Cardiovasc Surg 1990;99:264-268.[Abstract]
- Okumura N., Teramachi M., Takimoto Y., Nakamura T., Ikada Y., Shimizu Y. Experimental reconstruction of the intrathoracic trachea using a new prosthesis made from collagen grafted mesh. ASAIO J 1994;40:834-839.
- Suzuki T., Suzuki S., Kamio Y., Hori G. Closure with bronchial wall flap and omental pedicle of defect caused by dehiscence of tracheal suture line after extended right upper sleeve lobectomy. J Thorac Cardiovasc Surg 1996;112:1116-1117.[Free Full Text]
- Morgan E., Lima O., Goldberg M., Ferdman A., Luk S.K., Cooper J.D. Successful revascularization of totally ischemic bronchial autografts with omental pedicle flaps in dogs. J Thorac Cardiovasc Surg 1982;84:204-210.[Abstract]
- Yamanaka A., Kitano M., Tatsumi A., et al. An experimental study on regeneration of tracheal epithelium and gland. J Jpn Soc Bronhcol 1988;9:349-353.
- Nelson R.J., Goldberg L., White R.A., Shors E., Hirose F.M. Neovascularity of a tracheal prosthesis/tissue complex. J Thorac Cardiovasc Surg 1983;86:800-808.[Abstract]
- Kitada M. Study of revascularization of trachea graft in a canine autotransplantation model—a novel technique to promote blood supply to a long graft. J Jpn Assoc Thorac Surg 1996;44:2011-2018.
- Tomita M., Nakazone T., Taniguchi H., et al. Experimental evaluation of usefulness of omental wrapping at bronchial anastomosis. J Jpn Soc Bronchol 1988;10:270-274.
- Segalin A., Bonabina L., Carazzone A., Ceriani C., Peracchia A. Improving results of esophageal stenting: a study on 160 consecutive unresected patients. Endoscopy 1997;29:701-709.[Medline]
- Hind C.R.K., Donnelly R.J. Expandable metal stents for tracheal obstruction: permanent or temporary? A cautionary tale. Thorax 1992;47:757-758.[Abstract/Free Full Text]
- Nashef S.M.A., Dromer C., Velly J.F., Labrousse L., Couraud L. Expanding wire stents in benign tracheobronchial disease: indications and complications. Ann Thorac Surg 1992;54:937-940.[Abstract]
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Abstract
Introduction
