Ann Thorac Surg 1999;67:776-780
© 1999 The Society of Thoracic Surgeons
Original Articles
Removal of cartilage rings of the graft and omentopexy for extended tracheal autotransplantation
Katsumi Murai, MDa,
Hiroyuki Oizumi, MDa,
Toshiaki Masaoka, MDa,
Tsukasa Fujishima, MDa,
Masami Abiko, MDa,
Satoshi Shiono, MDa,
Yasuhisa Shimazaki, MDa
a Second Department of Surgery, Yamagata University School of Medicine, Yamagata, Japan
Accepted for publication July 15, 1998.
Address reprint requests to Dr Shimazaki, Second Department of Surgery, Yamagata University School of Medicine, Iida-nishi 2-2-2, Yamagata, 990-9585, Japan
e-mail: yshimaza{at}med.id.yamagata-u.ac.jp
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Abstract
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Background. One of the serious problems in longer-size tracheal transplantation is infection or severe stenosis of the graft, probably caused by an inadequate blood supply even with omentopexy. For obtaining an appropriate blood supply, we experimentally developed a new technique that included removal of some cartilage rings of the graft and omentopexy.
Methods. Twenty-one adult mongrel dogs were used. In group A (n = 11), a nine-cartilage ring length of the trachea in which six of nine rings were removed, leaving one cartilage ring at each end of the graft and another in the center, was autotransplanted with omentopexy. Two artificial tracheal rings outside the graft were used for maintaining the lumen. In group B (n = 10), a nine-cartilage ring length of the trachea was autotransplanted with omentopexy.
Results. In group A, all dogs survived until being sacrificed, whereas 5 group B dogs died of graft infection and mediastinitis (p < 0.05 versus group A). Mucosal blood flow of the graft in group A was normal and higher than in group B (p < 0.05). Grade of the graft stenosis at death or sacrifice was 14% ± 1% in group A and 58% ± 25% in group B (p < 0.05).
Conclusions. Removal of some cartilage rings improved blood supply to the graft and resulted in satisfactory survival and nonsignificant tracheal stenosis in extended tracheal autotransplantation.
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Introduction
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Using an omental pedicle flap is an effective way to supply an adequate blood flow to the transplanted trachea [1–5]. However, it may not provide sufficient blood flow to the graft when the graft is longer than eight cartilage rings or 4 to 5 cm, and the transplanted trachea may result in stenosis or infection [6, 7]. This could be caused by insufficient blood flow to the graft. Cartilage rings may interfere with the blood supply from the omental pedicle to the submucosal tissue of the graft. We therefore developed a new technique that included removal of some of the cartilage rings from the graft and securing the omental pedicle flap around the graft to make a direct attachment of the omentum to the tracheal submucosal tissue for obtaining an appropriate blood supply in longer tracheal transplantation. The aim of the present study is to clarify whether this technique provides adequate blood supply to the graft and results in avoiding significant stenosis in extended tracheal transplantation.
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Material and methods
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Twenty-one adult mongrel dogs weighing 9 to 12 kg were used. They received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and based on the "Guide for the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health (NIH publication 85-23, revised 1985).
After induction of anesthesia by an intravenous injection of 25 mg/kg pentobarbital sodium, intratracheal intubation and respiratory control were instituted. The upper abdomen was opened through a midline incision, and an omental pedicle flap was prepared. A right thoracotomy was done in the third intercostal space, and a nine-cartilage ring length of the mediastinal trachea was resected. All the dogs were divided into two groups. In the 11 dogs of group A, six of nine cartilage rings were completely removed, leaving one cartilage ring at each end of the graft and another in the center for facilitating anastomosis and maintaining the shape. To remove the cartilage ring from the graft, the perichondrium was incised along the center of the ring. Two small transverse cuts were made at both ends of the ring. Then the entire outer sheet of the perichondrium was detached from the ring with a small raspatory. The graft’s cartilage ring was exposed by these incisions, and it became easy to remove the cartilage ring from the graft. The resected trachea was autotransplanted and secured with 4-0 polypropylene continuous sutures (Prolene, Ethicon, Somerville, NJ). A silicone stent was placed in the graft lumen for maintaining its shape. To support the two portions without cartilage rings, a horseshoe-shaped 13- or 15-mm artificial cartilage ring made of hydroxyapatite (Asahi Kogaku Co, Yamagata, Japan) was placed outside the graft between the remaining cartilage rings and was not fixed. Therefore, two artificial rings were used in one dog. The entire graft including the anastomotic sites was covered with the omental pedicle flap (Fig 1). The stent was removed 1 week after the operation under a bronchoscope. In 10 dogs in group B, an ordinary tracheal graft with nine intact cartilage rings was autotransplanted with an omental pedicle flap. For 3 days after the operation, 10 mg of tobramycin was injected subcutaneously every day.
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Fig 1. A nine-cartilage ring segment of the intrathoracic trachea was excised (a). Six cartilage rings were completely removed from this excised trachea, and two cartilage rings at both ends and another at the midportion were left intact (b). The resected autograft was reimplanted with two horseshoe-shaped artificial rings between the remaining cartilage rings and it was covered with an omental pedicle flap (c). A silicone stent was placed inside of the graft.
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The grafts were observed at 1, 2, 3, 4, 6, 8, and 12 weeks after surgery. The epithelium of the graft was observed and the lumen size was classified into three groups according to Oizumi [8]; mild stenosis indicating an easy endoscopic passage (6 mm), moderate stenosis indicating a difficult passage, and severe stenosis indicating an impossible passage. In 6 dogs from each group, mucosal blood flow (MBF) was measured at the midportion of the graft and at the intact trachea about 2 cm proximal to the proximal anastomosis by using a laser flowmeter (Lasermeter ALF 21, Advance Co.). Five measurements were made at each site, and the mean of the three values after eliminating the highest and lowest values was defined as an actual measured value [9]. In each group, the autograft MBF and recipient MBF were presented as mean ± standard deviations. The grafts were examined histologically and the size of the graft was also measured at the time the animals died or were sacrificed. The internal diameter of the grafts was measured at the time of operation (a) and that of the stenotic site was done after death or sacrifice (b), and a cross-sectional area was calculated. The percentage of stenotic ratio (SR) of the graft was expressed as the following formula: 
When the animals were sacrificed, India ink was injected into the right gastroepiploic artery at a pressure of 150 mm Hg. The graft was then removed, fixed in a 10% formalin solution, and stained with hematoxylin and eosin. The midportion of the graft was microscopically studied.
Statistical analysis was done using a Mann-Whitney U test, defining p < 0.05 as a significant difference.
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Results
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Survivors
In group A, all animals (100%) survived until sacrificed at 3 to 21 months (10 ± 7 months)(Table 1). On the contrary, in group B, 4 animals died of mediastinitis that resulted from graft infection at 4 to 7 days after the operation, and another one died 6 weeks after operation of mediastinitis that was probably related to graft infection. Only 5 of the 10 animals (50% in group B (p < 0.05 versus group A) survived until sacrificed at 3 to 9 months (5 ± 2 months).
Endoscopic findings
In group A, a part of the epithelium was lost in 2 animals and was darkly discolored in 2 others 1 week after operation. However, these changes disappeared and were healed 2 to 3 weeks after removal of the stent. In the other animals in group A, the epithelium was well preserved until the animals were sacrificed. In group B, the epithelium was completely lost and the cartilage ring was exposed at death or 1 week after operation in all the animals. Macroscopic epithelial regeneration was found in the third or fourth postoperative week. Stenosis was not found in any animal of group A through 12 weeks after operation (Figs 2, 3). However, in group B, mild stenosis was noted at 8 weeks after operation in 4 of the 5 survivors, and in 3 of them, moderate stenosis was noted at 12 weeks after operation (Fig 3). In only 1 animal, the trachea tended to be flattened at the middle but was not stenotic.
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Fig 3. Bronchoscopic stenotic finding in long-term survivors. (- = none; + = mild; ++ = moderate; w = weeks.)
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Mucosal blood flow
In group A, autograft MBF was similar to recipient MBF through 12 weeks after operation (Fig 4A). However, in group B, autograft MBF was lower than recipient MBF at 1, 4, 6, 8, and 12 weeks after the operation (p < 0.05) (Fig 4B). At 1, 2, 4, 8, and 12 weeks after the operation autograft MBF was higher in group A than in group B (p < 0.05) (Fig 4C).
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Fig 4. Mucosal blood flow (MBF) of the graft and intact trachea. The MBF was measured at the midportion of the graft and at the recipient trachea 2 cm proximal to the anastomosis using a laser flowmeter. In group A, MBF of the graft was similar to that of the intact trachea through 12 weeks after operation. The MBF of the graft was lower than that of the intact trachea through 12 weeks after operation in group B (p < 0.05). Comparison of autograft AMBF between group A and B shows that autograft MBF was lower in group B than A through 12 weeks after operation (p < 0.05).
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Pathologic findings
Grade of stenosis of the graft, stenotic ratio, obtained at the time of sacrifice was 12% to 16% (14% ± 1%) in group A and 16% to 75% (58% ± 25%) in 5 long-term survivors in group B (p < 0.05) (Table 1). Histologic study revealed ciliary multilayered cylindrical epithelium of the mucous membrane and clear inflow of the injected India ink from the gastroepiploic artery into the submucosal vessels in group A (Fig 5).
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Fig 5. Normal epithelium and good neovascularization in submucosal area were seen in a trachea from group A.
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Comment
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The maximum length of successful tracheal autografting in experimental studies was eight cartilage rings [6] or 4 cm [7], even when it was covered with an omental pedicle flap. The experimental studies showed significant stenosis at the midportion of the graft that probably was caused by ischemia when the graft was longer than eight cartilage rings [6, 7]. The present method was effective for neovascularization, which restored blood flow to the submucosal tissue of the transplanted trachea well. This study also confirmed that the poor blood supply to the transplanted trachea resulted in graft failure in group B, and demonstrated that cartilage rings interfered with the blood supply from the omentum to the submucosal tissue of the graft and that all cartilage rings were not necessary for maintaining the shape in tracheal transplantation. Stenosis of the graft increased with time in 4 long-term survivors of group B, and even in the other long-term survivor of group B, the cartilage ring of the graft was atrophied. The present study suggests that an adequate blood supply would be helpful to prevent epithelial necrosis immediately after the operation and would avoid atrophy of the cartilage ring long after operation. The results in group B were poor. Most animals in group B were not studied before group A; therefore, there was no difference in technical proficiency and animal care between the groups. A stent was not used in group B dogs. There was some epithelial damage because of oppression by a stent in a few group A dogs. Not using a stent would not result in poor outcome in group B.
Recently, Yokomise and colleagues [10] reported a new method in which the graft was divided at the midportion and an omental pedicle flap was introduced there to improve blood flow in extended tracheal transplantation. We are concerned that there may be an increased omental prolapse into the lumen through the split when using their method, though they did not mention this factor. Although our method is slightly more complex compared with their method, there should be no possibility for the omentum to grow inside the graft.
An artificial tracheal ring made of hydroxyapatite was used for maintaining the shape in this study [8], and was useful to maintain the luminal structure. This ring was placed outside of the graft, and the graft with the rings was covered with an omental pedicle flap. No granulation tissue was found around the artificial tracheal ring, which was never dislodged or broken and which adhered to the omentum. The graft also adhered to the omental flap; therefore, the lumen was adequately maintained. However, an artificial tracheal ring was placed in one of the three removed cartilage rings. The present study demonstrated that cartilage rings interfered with the blood supply and that all the cartilage rings were not necessary for maintaining the lumen adequately. These findings suggest that the operative procedure could be further improved; for example, if one cartilage ring was removed and the other cartilage ring was left intact, an artificial ring might not be required.
Mucosal blood flow was measured by using a laser blood flowmeter, which has been frequently used because of its ease of use, high reproducibility, and noninvasiveness in other tissues [11, 12]. This method is reported to be useful to determine graft failure in organ transplantation [13–15]. Whether absolute values can be used to compare materials is controversial. Relative changes to the control may be appropriate for comparison [9]. However, in the present study, MBF as a control measured in the intact trachea in groups A and B were almost the same through 12 weeks after operation. Therefore, the absolute values of the blood flow were directly compared in groups A and B. Those values were higher in group A than B, suggesting that normal blood flow was obtained in group A, and less blood flow was supplied in group B. Mucosal blood flow measurements were performed in 12 of the 21 dogs. These were not done in the initial series of animals and in some animals that died early after the operation in group B. Therefore, MBF measurements in group B dogs were obtained from those with long-term survival. Had MBF been measured in all dogs, it may have been less in group B.
Results of the present study indicate that sufficient blood flow to the graft prevents epithelial loss and atrophy of cartilage rings. This method may enable a longer extension of tracheal transplantation.
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References
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Abstract
Introduction
