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Ann Thorac Surg 2000;69:1701-1706
© 2000 The Society of Thoracic Surgeons

Original articles: General thoracic

Revascularization of canine cryopreserved tracheal allografts

Hiroshi Moriyama, MDa, Tadahiro Sasajima, MD, PhDa, Satoshi Hirata, MDa, Kosuke Yamazaki, MDa, Eiji Yatsuyanagi, MDa, Yoshihiko Kubo, MD, PhDa

a First Department of Surgery, Asahikawa Medical College, Asahikawa, Japan

Address reprint requests to Dr Sasajima, First Department of Surgery, Asahikawa Medical College, 4–5 Nishikagura, Asahikawa 078–8307, Japan
e-mail: sasajit{at}asahikawa-med.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. We examined the blood supply of a cryopreserved tracheal allograft and its morphohistologic changes after transplantation.

Methods. In each of 22 dogs, a five-ring tracheal segment was replaced by one of the following tracheal grafts: fresh autografts (n = 8), cryopreserved tracheal allografts (n = 8), or fresh allografts (n = 6). The cryopreserved tracheal allografts were preserved at -196°C for 60 days. No immunosuppressant was given to any of the animals. All grafts were retrieved at 1 and 12 weeks and assessed by microangiography and histology.

Results. The epithelial denudation and the revascularization of the transverse intercartilaginous arteries were recognized within 7 days as common to each of the three types of grafts. In the cryopreserved tracheal allografts, neither cartilage degradation nor graft shrinkage occurred at 7 days. However, the recanalized transverse intercartilaginous arteries completely disappeared at 12 weeks, and marked shrinkage occurred; the cartilage cells were accompanied by karyolysis and were significantly decreased in number (p < 0.05). Recanalization of the transverse intercartilaginous arteries was also demonstrated in the fresh allografts; however, necrosis abruptly occurred as a result of acute rejection responses.

Conclusions. Cryopreservation of a tracheal allograft provided sufficient reduction of the acute rejection responses, and blood supply to the cryopreserved tracheal allograft was established through the recanalized transverse intercartilaginous arteries within 7 days; however, subsequent chronic rejection responses resulted in occlusion of the transverse intercartilaginous arteries and atrophy.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Although tracheal neoplasm and trauma are rare, the use of a tracheal graft is essential when such patients require long segmental replacement of more than 6 cm [1]. With this aim, tracheal allografts have been tested in animal models as the most feasible approach; however, fresh tracheal allografts have commonly failed because of airway stenosis or obstruction, in which the underlying process was graft collapse owing to cartilaginous micronecrosis caused by the acute rejection [2]. Hence, to reduce the rejection responses, immunosuppressive agents have usually been used in various types of allografting, although current improvement in cryopreservation technique has enabled allografts to be preserved for a long-term period and their alloantigenicity to be reduced sufficiently. Favorable results of cryopreserved allograft transplantation have been reported in the aortic valve [3], the aorta [4], the saphenous vein [5], skin [6], cartilage [7], and the trachea [8]; recent studies regarding cryopreserved tracheal allotransplantation in the use of animal models have also demonstrated encouraging results, suggesting the feasibility of immunosuppressant-free allotransplantation [8–10]. As to the beneficial effects of cryopreservation on a tracheal allograft, the majority of authors reported that the integrity of the subepithelial tissue and chondrocytes remained without any significant inflammatory cell infiltration for a long period after transplantation; they concluded that the cryopreserved tracheal allografts (CTAs) retained viability and continued functioning without any graft stenosis or rejection responses as observed in fresh allografts. However, these inspiring results have failed to provide definitive evidence proving the viability of the cryopreserved allograft.

In the present study, we examined the vasculature and blood supply of the CTA and quantitatively analyzed the morphohistologic changes in the graft after transplantation.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Method of tracheal replacement
Twenty-two randomly selected mongrel dogs of both sexes, weighing 10 to 17 kg (average, 14.4 ± 1.58 kg [SD]), were used in this study. Their care and use complied with the "Principles of Laboratory Animal Care" and the "Guide for the Care and Use of Laboratory Animals" (NIH publication 85–23, revised 1985).

Each animal was anesthetized with intravenous thiamylal sodium, intubated, and ventilated with 33% oxygen. The cervical trachea was exposed through a midline neck incision, and a five-ring tracheal segment, with a length of approximately 2 cm, was resected from the recipient animal; a tracheal graft was then interposed by end-to-end anastomoses with interrupted 3-0 polypropylene sutures. Neither immunosuppressants nor steroids were given to any of the animals during the observation period.

Procurement and preparation of tracheal grafts
The tracheal grafts were divided into the following three groups: group 1 (n = 8), fresh autogenous grafts; group 2 (n = 8), cryopreserved allografts; group 3 (n = 6), fresh allografts. In group 1, the resected tracheal segment was autogenously reimplanted into the original position; in groups 2 and 3, the tracheal grafts were obtained at autopsy from animals used in other experiments.

In group 2, the tracheal grafts harvested from donor animals were preserved in Roswell Park Memorial Institute’s Medium 1640 (RPMI-1640) solution containing 10% fetal calf serum, 10% dimethyl sulfoxide, and 5% N-[2-hydroxyethyl]piperazine-N'-[2-ethanesulfonic acid] buffer and frozen to -100°C by a programmed freezer, followed by cryopreservation in liquid nitrogen at -196°C for later transplantation. Each transplantation in this group was performed after cryopreservation for 60 days. Before the transplantation surgery, the CTAs were thawed in the buffer at 37°C, serially rinsed with the preserved solutions containing 7.5%, 5.0%, 2.5%, and 0% dimethyl sulfoxide, and then implanted into the recipient animals. Each of the graft specimens were subjected to a histologic examination immediately before implantation.

Graft surveillance, retrieval, and preparation
To check the graft viability, postoperative graft surveillance was performed by bronchoscopy 1, 2, 4, 8, and 12 weeks postoperatively. The grafts in groups 1 and 2 were retrieved at 1 and 12 weeks after transplantation as planned, whereas the grafts in group 3 were removed immediately after a fatal graft failure was found.

Microangiography was performed on each of the three grafts retrieved at 1 and 12 weeks in groups 1 and 2, and two grafts retrieved at 7 days in group 3, using the following methods: after anticoagulation with full-dose heparin, the animal was euthanized, and 40 mL of 120% weight/volume BaSO4 containing 0.5 g of gelatin was injected into the bilateral carotid arteries. After the tracheal microvessels were filled with the BaSO4 solution, the tracheal graft, including both anastomotic sites, was removed. The length of the retrieved graft was measured, and the graft was opened longitudinally at the membranous trachea for gross inspection of the luminal surface and then fixed with 10% natural buffered formalin for 24 hours. After fixation, xeroradiography of the graft was performed to obtain the microangiogram. All of the fixed grafts were cut longitudinally at the anterior wall, embedded in paraffin, longitudinally sectioned, and stained with the hematoxylin-eosin, alcian blue, periodic acid–Schiff, and toluidine blue methods.

Morphohistologic quantitative analysis
The number of the tracheal glands in the total area of each longitudinal section was microscopically counted and presented as the number per square millimeter of the tracheal submucosal area. The number of the tracheal cartilage cell nuclei was also microscopically counted in 10 randomly selected fields at a magnification of 100x, averaged for each section, and expressed as the number of nuclei per square millimeter of the tracheal cartilage area. Photomicrographs of all sections were taken, and a computerized morphometric analysis system (Macintosh, Apple Computer Inc, Cupertino, CA) with the public domain program "Image" (National Institutes of Health Research Service Branch, NIMH, Bethesda, MD) was used to measure the area of the tracheal glands that were observed in the submucosal area, which was presented in 100 square micrometers per square millimeter of tracheal submucosal area.

Statistical analysis
All data were expressed as mean ± one standard deviation and analyzed with the StatView software package (Abacus Concepts, Inc, Berkeley, CA). Differences between intervals in each group were tested by the Kruskal-Wallis test (nonparametric analysis of variance), and the paired Student’s t test was used to compare quantitative morphohistologic results before transplantation with those obtained 7 days or 12 weeks after transplantation. A p value less than 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Group 1
Bronchoscopic examination revealed no ischemic changes, and neither stenosis nor shrinkage were recognized. In each of the grafts retrieved at 7 days and 12 weeks after transplantation, microangiography clearly visualized the revascularized ladder-shaped intrinsic transverse intercartilaginous arteries (TIAs) of the graft as well as the recipient trachea, confirming that the revascularization between the graft and the recipient bronchial arteries was established as early as day 7 and that the patency of the graft TIAs was maintained for at least 12 weeks (Figs 1A, 1B). Histologically, extensive epithelial denudation was demonstrated at day 7; however, complete epithelial regeneration with cilia and functioning subepithelial glands containing mucus were recognized in the grafts 12 weeks after transplantation (Fig 2A). Graft shrinkage was not observed, and the morphohistologic integrity of the trachea was normally retained in each of the fresh autogenous grafts (Table 1).



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  		Fig 1. Microangiography of tracheal grafts. Fresh autogenous grafts 7 days (A) and 12 weeks (B) after transplantation, showing the presence of transverse intercartilaginous arteries. Cryopreserved allografts at 7 days (C) and 12 weeks (D) after transplantation. Cryopreserved allograft at 7 days indicated a newly developed microvasculature surrounding the graft and the presence of transverse intercartilaginous arteries, which disappeared after 12 weeks. (E) Fresh allograft 7 days after transplantation, showing recanalized transverse intercartilaginous arteries. Graft is shown between black or white narrow arrows; transverse intercartilaginous arteries are shown by white or black wide arrows.

 


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  		Fig 2. Histologic comparison between tracheal grafts 12 weeks after transplantation. (A) Fresh autogenous graft, showing complete epithelial regeneration with cilia, functioning subepithelial glands containing mucus (white wide arrows), recanalized transverse intercartilaginous arteries (black narrow arrows), and no graft shrinkage. (B) Cryopreserved allograft, revealing obvious decreases in cartilage cell number and small vessels containing the BaSO4 (black arrows), a simple squamous epithelial lining, and an absence of tracheal subepithelial glands. (C) Cryopreserved allograft, demonstrating overlapping cartilage collocation as a result of the marked longitudinal shrinkage. (Longitudinal section, alcian blue stain; x40, bar = 100 µm in A and B; x5, bar = 1 mm in C.)

 

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  		Table 1. Morphohistologic Changes in Grafts After Transplantation

 
Group 2
The CTAs immediately before transplantation maintained the morphohistologic integrity of the trachea. However, the cartilage cells decreased in number for the duration of the cryopreservation period (Table 2). Bronchoscopic examination found no ischemic changes, and neither stenosis nor shrinkage were macroscopically perceived during the study interval. The microangiography showed the recanalized TIAs of the grafts 7 days after transplantation to be the same as in the autogenous grafts (Fig 1C); however, these arteries had completely disappeared in the 12-week grafts, and abundant newly developed microvasculatures surrounding the graft were visualized (Fig 1D). Histologically, extensive epithelial denudation and subepithelial glands filled with mucus were observed, and neither cartilage cell degradation nor graft shrinkage occurred in the same manner as in the autogenous grafts 7 days after transplantation. However, in each of the CTAs retrieved at 12 weeks, although no stenosis was recognized bronchoscopically, a marked longitudinal shrinkage occurred (Table 1), and their longitudinal sections clearly demonstrated an overlapping cartilage collocation as a result of the shrinkage (Figs 2B, 2C). These cartilage cells had significantly decreased in number and were commonly accompanied by swelling or karyopyknosis followed by karyolysis (Table 1). Small vessels containing the BaSO4 were rarely found in the intercartilaginous tissue. The luminal surface at the anastomotic sites was covered with pseudostratified columnar epithelium, although the middle portion of the graft was lined with simple squamous epithelium. No cilia were recognized in either type of epithelium, and the tracheal subepithelial glands had disappeared (Table 1; Fig 2B). These findings suggested slow, ongoing atrophic changes.


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  		Table 2. Influence of Cryopreservation on Tracheal Cartilage Cells

 
Group 3
Of the six fresh allografts, four were euthanized ahead of schedule because of severe respiratory distress caused by graft stenosis, whereas the remaining two, retrieved at 7 days as planned, retained their function, and microangiography revealed the recanalized TIAs (Fig 1E). Histologically, the epithelial denudation also occurred in the same manner as in those seen in groups 1 and 2; the morphohistologic tracheal integrity was retained up to day 7, although a mild immunologic reaction was recognized. Bronchoscopically, the remaining four grafts also showed a viable mucosal appearance up to day 7; however, necrosis abruptly occurred as a result of acute rejection responses, resulting in obligatory removal at 2 to 3 weeks after surgery. The skeleton tracheal cartilage rings were obtained at autopsy as the remnant of the necrotic graft, and the histology showed micronecrosis and karyolysis of cartilage cells.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
In respect to the influence of cryopreservation on the tracheal structural integrity, Deschamps and colleagues [11] reported experimental results of cryopreserved autogenous tracheal grafts, in which smooth muscle cells, epithelium with functional cilia and mucus production, and the horseshoe-shaped cartilage retained their integrity and viability, without any disruption of the architecture; these findings did not change during cryopreservation of more than 30 days. The present study also showed that the cartilage cells did not decrease in number up to 30 days; however, significant reduction was recognized in the grafts after 60 days of cryopreservation, suggesting that progressive cold injury may result in graft degradation after a long-term period of cryopreservation.

Tice and Zerbino [12] reported that cryopreservation yields a significant reduction in alloantigenicity, whereas Rose and associates [13] demonstrated in a detailed study using immunologically well-defined individuals that the trachea itself revealed weak rejection responses even in the presence of major histoincompatibility. Hence, the cryopreservation may further weaken the intrinsically low organ-specific antigenicity of tracheal allografts. With this background, it has been reported that CTAs were macroscopically and histologically viable without any immunologic rejection responses, and that their structural integrity was maintained for a long-term period after implantation [8–10]. However, in that case, the blood supply to the CTAs and the influence of the probable retention of low-grade alloantigenicity on the fate of the long-term graft have not been investigated.

In the present study, we observed within 7 days after implantation two definitive pathologic changes as common findings of the three different types of tracheal graft, ie, the epithelial denudation and the revascularization of TIAs. The epithelial denudation of the tracheal grafts occurring within 7 days after transplantation was thought to be caused by surgical injury, as in the case of the vascular grafts [14]; this coincides with the results of other reports [15]. The early phase revascularization of TIAs was confirmed in another implantation study of autogenous tracheal grafts [16], whereas in the present study, microangiography and histology demonstrated that the revascularization in the two types of allograft also occurred within 7 days after transplantation and that the revascularization may occur even in the fresh allografts, ie, in the early phase before the regular immunologic response was provoked.

In the secondary process, the three types of tracheal grafts represented obviously different biologic behavior. The autogenous grafts had retrieved their intrinsic structural integrity in the secondary process, whereas more than half of the fresh tracheal allografts were destroyed by severe rejection responses, which was considered to be caused by the acute rejection as observed at 2 to 3 weeks after transplantation. Regarding the immunologic responses of CTAs, Mukaida and coworkers [17] also reported that allografts that had been cryopreserved for 7 days showed a positive expression of the major histocompatibility complex class II antigen and developed necrosis after transplantation, whereas neither necrosis nor expression of the antigen was recognized in allografts with 1 to 6 months cryopreservation. However, in our results, microangiography 12 weeks after transplantation showed an extensive occlusion of the TIAs, and, histologically, a marked longitudinal shrinkage with fibrosis, disappearance of the subepithelial glands, and karyopyknosis followed by karyolysis of the cartilage cells were recognized. These results suggest that the CTAs were slowly but progressively degraded after implantation, and that the occlusion of the TIAs was thought to be a result of the rejection responses to the endothelial cells as in the failure of the vascular allografts in the secondary process [14].

From the present results, the fate of the CTA is here summarized: revascularization and epithelial denudation of the grafts occur within 7 days after transplantation as the first process, and a pseudoepithelial lining covers the luminal surface in the secondary process; however, subsequent mild but chronic rejection responses bring about occlusion of the recanalized TIAs, resulting in the degradation and shrinkage. Nevertheless, the marked differences in the healing process and the biologic fate between the fresh graft and the CTAs proved the efficacy of cryopreservation for reducing alloantigenicity, and thus the CTA may be useful for patients with a short tracheal defect. However, further long-term studies will be necessary to prove whether the CTA is suitable even for patients with a very long segmental defect.

In conclusion, cryopreservation of a tracheal allograft provides sufficient reduction of the acute rejection responses for maintaining a satisfactory function as an airway conduit, and the blood supply to the graft through the recanalized TIAs is established in the early phase after implantation; however, mild but chronic rejection responses continue, resulting in occlusion of the TIAs and consequent progressive atrophy.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Grillo H.C. Reconstruction of the trachea. Thorax 1973;28:667-679.[Abstract/Free Full Text]
  2. Nakanishi R., Shirakusa T., Hanagiri T. Early histopathologic features of tracheal allotransplant rejection. Transplant Proc 1994;26:3715-3718.[Medline]
  3. O’Brien M.F., McGiffin D.C., Stafford E.G., et al. Allograft aortic valve replacement. Long term comparative clinical analysis of the viable cryopreserved, and antibiotic 4°C stored valves. J Cardiac Surg 1991;6:534-543.[Medline]
  4. Kirklin J.K., Smith D., Novick W., et al. Long-term function of cryopreserved aortic homografts. J Thorac Cardiovasc Surg 1993;106:154-166.[Abstract]
  5. Gelbfish J., Jacobowitz I.J., Rose D.M., et al. Cryopreserved homologous saphenous vein. Ann Thorac Surg 1986;42:70-73.[Abstract]
  6. Hirase Y., Kojima T., Takeishi M., Hwang K.H., Tanaka M. Transplantation of long-term cryopreserved allocutaneous tissue by skin graft or microsurgical anastomosis. Plast Reconstr Surg 1993;91:492-501.[Medline]
  7. Hartog J.M., Slavin A.B., Kline S.N. Reconstruction of the tempomandibular joint with cryopreserved cartilage, and freeze-dried dura. J Oral Maxillofac Surg 1990;48:919-925.[Medline]
  8. Yokomise H., Inui K., Wada H., Ueda M., Hitomi S. Long-term cryopreservation can prevent rejection of canine tracheal allografts with preservation of graft viability. J Thorac Cardiovasc Surg 1996;111:930-934.[Abstract/Free Full Text]
  9. Mukaida T., Shimizu N., Aoe M., et al. Experimental study of tracheal allotransplantation with cryopreserved grafts. J Thorac and Cardiovasc Surg 1998;116:262-266.[Abstract/Free Full Text]
  10. Tojo T., Niwaya K., Sawabata N., et al. Tracheal replacement with cryopreserved tracheal allograft. Ann Thorac Surg 1998;66:209-213.[Abstract/Free Full Text]
  11. Deschamps C., Trastek V.F., Ferguson J.L., et al. Cryopreservation of canine trachea. Ann Thorac Surg 1989;47:208-212.[Abstract]
  12. Tice D.A., Zerbino V. Clinical experience with preserved human allografts for vascular reconstruction. Surgery 1972;72:260-267.[Medline]
  13. Rose K.G., Sesterhenn K., Wustrow F. Tracheal allotransplantation in man. Lancet 1979;24:433.
  14. Azuma N., Sasajima T., Kubo Y. Immunosuppression with FK506 in rat arterial allografts. J Vasc Surg 1999;29:694-702.[Medline]
  15. Nakanishi R., Shirakusa T., Takachi T. Omentopexy for tracheal autografts. Ann Thorac Surg 1994;57:841-845.[Abstract]
  16. Kitada M. Study of revascularization of tracheal graft in canine autotransplantation model. A novel technique to promote blood supply to a long graft. J Jpn Assoc Thorac Surg 1996;44:2011-2018.
  17. Mukaida T., Shimizu N., Aoe M., Ando A., Date H. Tracheal allotransplantation after varying terms of cryopreservation. Transplantation Proc 1998;30:397-400.[Medline]
Accepted for publication December 11, 1999.




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