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Ann Thorac Surg 1997;64:199-202
© 1997 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Successful Tracheal Autotransplantation With Two-Stage Approach Using the Greater Omentum

Department of Cardiothoracic Surgery, The First Hospital of Beijing Medical University, Beijing, China

Accepted for publication January 4, 1997.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. Although many studies on reconstruction of extensive circumferential tracheal defects with a segmental trachea have been done, up to date, no reliable and satisfactory tracheal transplantation procedure has been developed. We conducted this experiment to investigate feasibility and efficacy of a staged tracheal transplantation approach for tracheal reconstruction.

Methods. Twelve dogs were divided equally into groups I and II. A segment of cervical tracheas (six rings) was harvested as an autograft and implanted heterotopically into the greater omentum. Two weeks later, the autografts with their omental pedicles were transplanted orthotopically to the cervical (group I) or the thoracic portion of the trachea (group II). Bronchoscopic examination were performed monthly during a 5-month follow-up period. After sacrificing the dogs, we had the grafts examined macroscopically and microscopically.

Results. The dogs of both groups survived well until the end of the follow-up. No abnormal findings were observed through bronchoscopy. The grafts had normal appearance, without shrinkage, granulation, or necrosis by postmortem gross examination. Histologic examination showed the structures of the grafts were intact.

Conclusions. We conclude that the two-stage tracheal transplantation approach using the greater omentum is feasible, and can facilitate the survival of a tracheal graft as well.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
At present, more than half of the human abnormal trachea can be resected, then reconstructed with primary end-to-end anastomosis. However, extensive circumferential tracheal resection is occasionally required in patients with primary or secondary malignant tracheal diseases or with benign stenosis of the trachea due to trauma, inflammatory, or iatrogenic causes [1]. When such an extensive circumferential tracheal resection is performed, perhaps a terminal tracheal fistula is the only safe method that can be adopted for patients because considerable difficulties are encountered in the field of reconstruction of extensive circumferential tracheal defects with tracheal substitutes. Many prosthetic grafts [2–4] and tissue grafts [5–7] have been tried extensively to repair such tracheal defects, but only limited success has been achieved. With the belief that a tracheal graft, possessing the native epithelium and cartilaginous ring, might be best for repairing tracheal defects if the problems of revascularization and immunorejection were solved, many investigators have conducted studies on tracheal transplantation [8–17]. Most of the studies did not have successful results either. It is commonly agreed that tracheal graft ischemic necrosis was the major cause of the failure results of the studies.

It is clear to all that no vascular pedicle is available for direct microsurgical anastomosis to provide early revascularization for a tracheal graft; moreover, the airway is susceptible to infection. These disadvantageous factors contribute to the fact that it is very difficult to prevent ischemic necrosis of a tracheal graft. To revascularize indirectly tracheal graft as early as possible, some investigators [12–15] introduced omentopexy to the field of tracheal transplantation, and had improved results. However, in the results they reported, not all of the tested grafts survived. Moreover, Nakanishi and associates [15] reported that there is a limitation to tracheal transplantation with omentopexy. In their studies, 11 of 13 transplanted tracheal autografts longer than 3.5 cm or more than seven cartilage rings suffered from ischemic malacia or disintegration of cartilage. It is evident that the one-stage tracheal transplantation procedure, tracheal transplantation with omentopexy, is not perfect. Recently, some reports [16, 17] showed that it is more reasonable to adopt a two-stage approach than a one-stage approach for tracheal transplantation because direct revascularization of the tracheal graft cannot be performed.

In our pilot study [18], we found that it is more effective for tracheal graft revascularization to implant the tracheal graft heterotopically into the greater omentum than to reimplant the tracheal graft orthotopically with omentopexy, and there was no adhesion in the peritoneal cavity where the tracheal graft was implanted into the greater omentum. We deduced that it would be feasible and more effective for the survival of tracheal graft if a two-stage approach were used for tracheal transplantation. In the present experiment, we also used tracheal autografts to avoid immunorejection and investigated the feasibility and efficacy of the two-stage tracheal transplantation approach, ie, tracheal reconstruction with a revascularized tracheal graft that was first implanted heterotopically into the greater omentum for revascularization.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Twelve adult mongrel dogs weighing from 15 to 20 kg were anesthetized with intravenous injection of pentobarbital sodium (20 mg/kg) and were placed in the supine position. Then oral intubation were performed and the tube was connected to a pressure-limiting respirator. Additional anesthetics were administered throughout the procedure if needed. The dogs were operated on in the manner described below.

Operative Procedure
STAGE I: TRACHEAL GRAFT IMPLANTED HETEROTOPICALLY INTO THE GREATER OMENTUM.
After a midline cervical incision was made, a six-ring segment of the trachea was excised and immersed in physiologic saline solution containing penicillin G (200 U/mL). Intubation into the distal portion of the trachea was carried out across the operative field with a sterile tube for ventilation. Tracheal reconstruction was performed by end-to-end anastomosis with interrupted silk sutures. After a small middle laparotomy, the greater omentum was brought out of the peritoneal cavity. The tracheal autograft was embedded into the lower portion of the greater omentum. During the process, care was taken to avoid talc and unnecessary foreign materials being left in the peritoneal cavity. All incisions were closed in layers.

STAGE II: ORTHOTOPIC TRACHEAL TRANSPLANTATION USING THE REVASCULARIZED TRACHEAL GRAFT WITH ITS OMENTAL PEDICLE.
Two weeks later, according to a timetable that was scheduled according to the findings of our previous study [18], the dog was reanesthetized and oral intubation was performed and connected to a pressure-limiting respirator. Through an upper midline incision, the abdomen of the dog was reopened. The graft was found and the lumen of the graft was opened. Then, a laser Doppler flowmeter (Periflux PF3, Stockholm, Sweden) was used to monitor the mucosal blood flow of the tracheal graft, and the greater omentum with the graft in its tip was dissected from the spleen and the left edge of the stomach; only the right gastroepiploic arteries were preserved, as our previous study reported [18]. After the fourth intercostal incision was made, the tracheal autograft with the omental pedicle was brought to the cervical area through the right thoracic cavity by a diaphragmatic defect in 6 dogs (group I) and to the thoracic cavity by a diaphragmatic defect in 6 dogs (group II). The cervical or thoracic trachea was transected and a sterile endotracheal tube was positioned in the lower trachea for ventilation. Then the tracheal autograft with the greater omental pedicle was transplanted interpositionally into the same dog's trachea. The upper anastomosis was first sutured, then the membranous portion of the lower anastomosis was completed similarly. The lower anastomosis was completed after the oral endotracheal tube was inserted across both upper and lower anastomoses. Finally, the cervical, the thoracic, and the abdominal incisions were closed in the usual fashion.

Examinations with a fiberoptic bronchoscope (BF 3; Olympus, Tokyo, Japan) were performed monthly until the animals were put to death on postoperative day 150. The grafts then were removed for macroscopic and microscopic studies.

Postoperative Care
Dogs were given 1 million units of penicillin G intramuscularly per day for 3 postoperative days. All animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985).

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
All dogs from the two groups survived very well after the operations until they were put to death. Follow-up fiberoptic bronchoscopy revealed that the lumens were patent without necrosis or granulation. Macroscopic study showed that the grafts had no shrinkage or malacia and the cartilage rings of all the grafts were intact. Light microscopic study demonstrated that all the grafts had normal multilayered epithelium and cartilage.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Experimental reconstruction of extensive circumferential tracheal defects with tracheal grafts has been done for more than four decades [8–18]. However, with few exceptions, these experiments were unsuccessful. Some reports on tracheal autotransplantation have been published. In 1950, both Daniel and colleagues [8] and Ferguson and colleagues [9] published their results of a series of studies in dogs in which three-ring tracheal autografts were implanted immediately or implanted after tracheal graft preservation. In their experiments, necrosis or severe stenosis developed in all of the tracheal autografts within 1 month. Neville and associates [10] reported that when autografts containing three tracheal rings were immediately reimplanted, the lumens were patent but the cartilage was absorbed. When five-ring grafts were implanted, dissolution of the cartilage and stenosis of the airway were seen. In these studies, in which immunorejection was not a factor, the unsuccessful results were evidently due to graft ischemia, and indicated that outgrowth of the collateral circulation from the recipient tracheal and mediastinal tissue to tracheal graft could not maintain the integrity of the grafts.

In 1982, Morgan and associates [19] reported that application of the greater omental flap to an avascular bronchial autograft 2 cm long resulted in early revascularization and prevented necrosis of the bronchial graft. Ever since that, research on tracheal transplantation has been rekindled. Various wrapping procedures, such as with sternocleidomastoid muscle [11], the greater omentum [12–15], or a fascial flap [16, 17], have been applied extensively to experimental tracheal transplantation. The majority of the studies were done with tracheal grafts that were isolated and reimplanted immediately, then wrapped by the transported greater omental pedicle flap, and demonstrated a reduced incidence of tracheal graft failure. However, an experimental study by Nakanishi and associates [15] showed that only some of the tracheal autografts shorter than 4 cm wrapped by the omental flap could survive; if the grafts were longer than 4 cm, the midportions of all the autografts suffered from malacia. By the study of silicone rubber injection, it was found that the blood supply of the graft with omentopexy was derived from two sources: the neovascularity from the recipient trachea at both ends of the graft and the supply from the greater omentum. From these findings, Nakanishi and associates considered that only the synergistic effects of the two supplies succeeded in preserving the viability of the graft at both ends near the anastomosis. The midportion of the autograft failed to receive the synergistic effect and become necrotic.

In the field of tracheal transplantation, direct revascularization of donor tracheal graft by microsurgical technique can not be expected because both the tracheal arteries and veins are numerous and very fine. Indirect revascularization of the tracheal graft may be the only method available. In any case, by indirect revascularization, neovascularity of the tracheal graft must be formed with a step-by-step process. This means also that the tracheal graft must experience a period of ischemia. Therefore, during the process of tracheal graft revascularization, it is of the utmost importance to have a close and immobile contact between the graft and its surrounding vascular bed. Otherwise, the time lag of tracheal graft revascularization will increase and lead to tracheal graft failure. By a one-stage tracheal transplantation procedure, eg, tracheal transplantation with omentopexy, the tracheal graft cannot become immobile because some vital movement, such as respiration, cough, or swallowing action, cannot be stopped. To reduce the time lag of tracheal graft revascularization, some investigators began to study two-stage tracheal transplantation approaches. Rose and associates [11] reported the only successful clinical tracheal allotransplantation. They placed a ten-ring allograft in the bed of the recipient's sternocleidomastoid muscle for 3 weeks. An eight-ring abnormal trachea of a 21-year-old male patient was replaced by the graft with the muscular pedicle. Delaere and associates [16, 17] conducted a series of experimental two-stage tracheal transplantations on rabbits using fascial flap, and showed successful results. In the procedure they adopted, the tracheal graft was implanted heterotopically into the lateral thoracic fascia (first stage) for revascularization, then transplanted orthotopically into the trachea (second stage). They found that the optimal time for the second-stage operation was 16 to 20 postoperative days.

We chose the greater omentum as a vascular vehicle for revascularization of tracheal autograft because it possesses not only a rich vascular network, but also a rich lymphatic network, and it is easy to extend. It has been applied to various situations to establish new arterial, venous, and lymphatic communications and to promote repair in areas of poor healing [20–22]. Besides these, some facts imply that the greater omentum may be the most powerful tool for successful revascularization of tracheal graft if the graft is implanted heterotopically into it. For example, the study by Nakanishi and associates [14] showed that all of the tracheal grafts embedded into greater omentum survived. In our previous studies [18], we embedded tracheal autografts heterotopically into the greater omentum and found that the tracheal autografts could revascularize well at 14 postoperative days, and no adhesion formed in the peritoneal cavity after the first operation. Encouraged by these results, we began to investigate the possibility and efficiency of tracheal reconstruction with a two-stage tracheal transplantation approach using the greater omentum. The findings of the present study that all animals of the two groups could endure the operation and all the grafts survived suggest that tracheal transplantation with the combined hetero-orthotopic approach using greater omentum is feasible and effective. This two-stage tracheal transplantation model might be adopted to further studies on tracheal allotransplantation.

In conclusion, this two-stage tracheal transplantation approach-embedding a donor tracheal graft heterotopically into the greater omentum for revascularization (first stage), waiting 2 weeks, and reconstructing the tracheal defect with the revascularized donor tracheal graft after forming the omental pedicle flap with the donor tracheal graft at its tip (second stage)-can facilitate the survival of tracheal grafts. This approach also can be used to repair defects of any portion of the tracheal if the immune problems can be solved.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Address reprint requests to Dr Li, Department of Cardiothoracic Surgery, The First Hospital, Beijing Medical University, No. 8 Xishiku Str, Beijing 100034, China.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Li, J. Articles by Chen, H. Search for Related Content PubMed PubMed Citation Articles by Li, J. Articles by Chen, H.