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Circumferential tracheal replacement with costal cartilage
J
THoRAc CARDIOVASC SURG
1987;94:175-80
Circumferential tracheal replacement with costal cartilage Long-termincorporation of foreign material or tissue in circumferential tracheal replacement will lead to progressive growth of granulation tissue, provoking either airway stenosis or a reduction of subepithe6al blood supply and thereby preventing the appearance of functioning ciliated epithelium in the replaced segment In experience with dogs, a 5 cm length of the thoracic trachea was replaced circumferentially with fresh autogenous untreated circularly positioned cartilage-perichrondrlum strips. During the period of strengthening of this neotracheal wall, a temporary tracheal prosthesis made of tubular siliconerubber withabsorbablesewing rings of polyglactin910 placed 3 mm from the end of the tube servedas a tracheal replacement Six months after the cartilage transplantation, the neotracheal wall had stabilized sufficiently for the siliconerubber tube to be extracted with an endoscope. Four weeks after extraction of the silicone rubber tube the neotracheal segment was completely covered with ciliated epithelium over a thin subepithelial, weD-vascularized layer. Subepithe6al vessels had a diameter of 180 ~m. They were a continuation of the intercartilaginous main vessels of the neotracheal wall. The presenceof normal cilia on the epithelium was proved through transmission electron microscopy. Even the tubules of the cilia were arranged in the right order. In the ink test, movement of the transport marker across the neotracheal segmentat a speed of 18 to 21 mm/min was proof of mucociliary clearance. In a process of migration starting from the margin of the trachea, the ciliated epithelium pervaded and replaced the preexisting temporary one-layer stratified squamous epithelium. This completely new technique of circumferential tracheal replacement with autogenous cartilage, avoiding permanent incorporation of foreign material, succeeds witbinthe observation period of up to 7 months.
Franz Eckersberger, M.D. (by invitation), Erich Moritz, M.D. (by invitation), and Ernst Wolner, M.D. (by invitation), Vienna, Austria Sponsored by Thomas W. Shields, M.D., Chicago, Ill.
EreqUisites for the clinical application of a technique for long-term replacement of a segment of trachea are the mechanical stability of the neotrachea and the complete covering of the lumen with ciliated epithelium in the absence of granulation tissue. We have tried to develop a circumferential tracheal replacement by transplanting autogenous fresh untreated cartilage for the production of a neotrachea to avoid permanent incorporation of foreign material. While the neotrachea consisting of transplanted cartilaginous tissue was allowed to strengthen, a silicone rubber prosthesis was implanted. Becauseabsorbable sewing rings were used, this prostheFrom the II. Surgical Clinic, University of Vienna, Vienna, Austria. Read in part at the Sixty-sixth Annual Meeting of The American Association for Thoracic Surgery, New York, N. Y., April 28-30, 1986. Address for reprints: Franz Eckersberger, M.D., II. Surgical Clinic, University of Vienna, Spitalgasse 23, A-1090 Vienna, Austria.
sis transformed itself into a tubular stent within the neotrachea, which could be extracted endoscopically. A$ there are no publications describing the transplantation of a cartilage-perichondrium strip into the mediastinum, experience had to be gathered from previous experiments to work out the optimum device for transplantation in relation to the required stability and to define the position of the perichondrial side of the transplant that would achieve long-term vitality of the cartilaginous tissue.
Material and methods A tracheal prosthesis 5.6 em long was fabricated from a silicone rubber tube* with a wall thickness of 1.5 mm (Fig. 1). The sewing rings were sutured 3 mm from the end of the tube with a polyglactin 910 running suture. *Silastic sheeting; reinforced, medical-grade silicone rubber; Dow Corning Corporation, Midland, Mich.
175
176 Eckersberger, Moritz, Wainer
Fig. 1. Temporary tracheal prosthesis with subterminal sewing rings that consisted of absorbable polyglaetin 910. Within 70 days the prosthesis is changing to a tube of silicone rubber stenting the neotracheal wall with the possibility of being telescoped into the native trachea.
These rings consisted of three circular layers of a polyglactin 910 band. * After right thoracotomy and resection of 5 em of the thoracic trachea, this tracheal prosthesis was interposed in mongrel dogs weighing 26 to 34 kg. The operation, performed with standard anesthesia, was done according to the method described by Neville, Bolanowski, and Soltanzadeh.' Free fresh autotransplant tissue made of costal cartilage was positioned circumferentially around this prosthesis and the ends of the strips were connected with an absorbable 4-0 polyglactin suture to produce a ring of strips around the prosthesis (Fig. 2, A and B). These transplants were taken immediately before transplantation from the partially resected cartilaginous part of the seventh and eighth ribs on the right side near the sternum after preparation with a scalpel (Fig. 3). The time between preparation and transplantation was less than 1 hour in all cases. The mediastinal pleura around these transplants was reconstructed so that it would close. Thus the mediastinal tissue was wrapped about the transplants for nutrition. Cartilage-perichondrium chips (3 mm in width, 1.5 em in length), cartilage-perichondrium strips (3 mm in width, 8 em in length), and cartilage-bone chips (3 mm in width, 2 em in length) were used for transplantation. The transplants were between 2 and 3 mm thick. The perichondrium was positioned partly about the prosthe*Vicryl band, 3 mm; Ethicon, Inc., Somerville, N. J.
The Journal of Thoracic and Cardiovascular Surgery
Fig. 2. A, Fresh free autotransplants of cartilage-perichondrium stripswereusedin long-term experiments. Theycovered the implanted tracheal prosthesis in circumferential rings. The perichondrial side of the transplants was positioned on the outer, cutting surface of the prosthesis. B, The ends of the strips were connected with an absorbable 4-0 polyglactin suture producing a ring of strips around the prosthesis. sis and partly adjacent to the nutritive mediastinal tissue. For every experiment four different sizes of prosthesis with diameters of 15,17,19, and 21 mm were prepared to ensure that the implanted prosthesis would be perfectly fitted to the diameter of the trachea. A 3-0 Prolene suture secured the prosthesis at the cranial margin of resection of the trachea to prevent dislocation of the silicone rubber tube after absorption of the sewing rings. The animals were divided into two groups. Group I. Five animals were electively put to death 6 to 9 weeks after cartilage transplantation to assess the vitality of the transplants. Vitality was judged with the use of a light microscope' and delineated in percent of specimens as a means of comparison. Group II. Group II comprised nine dogs used for long-term experiments. Stabilization and vascularization of the neotracheal wall were examined as was the epithelial covering of the lumen after extraction of the silicone rubber tube. Bronchoscopic examinations were performed regularly. Before extraction of the silicone rubber tube with a biopsy forceps, the Prolene suture was cut through with an endoscopy scissors. For extraction, the silicone rubber tube was telescoped in the rigid bronchoscope and the two were removed together. Transmission electron microscopic examination of epithelial biopsy tissue followed 4 weeks, 2 months, and 4 months after extraction of the silicone rubber tube. The function of mucociliary
Volume 94 Number 2 August 1987
Fig. 3. Transplant strips were preparated with the scalpel from the cartilaginous part of two ribs. The bony central part was not used in long-term experiments. In this way, each transplant had a cutting surface side and a perichondrial side.
Circumferential tracheal replacement
17 7
Fig. 4. After the mediastinal pleura was split, the mediastinal tissue was divided so that the main vessels were saved for a well-vascularized bed for the transplants.
clearance was tested by blowing dry ink particles (diameter 20 to 80 JLm) into the region of tracheal bifurcation of the anesthetized, spontaneously breathing animal followed by documentation of the transport speed of the marker with endoscopic photographs taken at intervals of 10 seconds. All animals received humane care in compliance with the Austrian "Law of Animal Experiments."
Results
Group I. Cartilage-bone transplants retained the least vitality. The bony part of the transplants had devitalized areas at regular intervals. The chip transplants retained the highest vitality: Dislocation of the chips was observed, however, which means the stability required for the trachea did not seem ensured. Those transplant strips whose perichondrial surface had been transplanted adjacent to the mediastinal tissue showed greater vitality than those cartilage-perichondrium strips that had been transplanted with the perichondrium over the tracheal prosthesis and the cutting surface of the preparation positioned adjacent to the mediastinal tissue (Fig. 4). Group II. In further long-term experiments based on this knowledge,only cartilage-perichondrium strips were used with perichondrium positioned adjacent to the mediastinal tissue; the cutting surface of the scalpel was thus superimposed on the tracheal prosthesis to the silicone rubber tube. We have also observed that the diameter of the tracheal prosthesis must be 2 to 3 mm smaller than the diameter of the trachea, so as to leave a split for invagination between the trachea and silicone rubber tube. The latter permitted telescope-like invagination of the tube into the trachea from the thirty-fifth day after tracheal replacement onward. This split for invagination enabled the epithelium to migrate from the
Fig. 5. Photographs taken through a Storz telescope 9 weeks after implantation of a prosthesis.The outer diameter was the same as that of the native trachea. As a result, no telescoping and migration of the epithelium was possible.A fold of mucosa was seen at the end of the silicone rubber tube.
margin of the native trachea while the silicone rubber tube was still in its position. If the diameter of the tracheal prosthesis was equal to that of the trachea, no epithelial migration from the margin of the trachea into the surface of the neotrachea could be observed. On the contrary, a fold of mucosa (Fig. 5) appeared at the margin of the trachea disrupting the ciliated epithelium at the margin of the neotrachea. The latter was homogeneously lined with substituting squamous epithelium, as we have seen in three dogs. The same occurred in two dogs when the prosthesis was smaller in diameter than the native trachea but the wall of the neotrachea was devitalized. Subtotal airway stenosis occurred in 1 to 12 days after extraction of the silicone rubber tube because of granulation tissue and malacia of the neotracheal segment. There was only an
The Journal of
1 7 8 Eckersberger, Moritz, Wolner
Thoracic and Cardiovascular Surgery
Fig. 6. Photographs of the neotracheal segment 4 months after extraction of the silicone rubber tube during the ink test to check the mucociliary clearance function. Spiral transportation form of the dry marker particles is observed even in the neotracheal segment. Time interval between left and right is 30 seconds. During this time, a test marker was transported 11 mm in the cranial direction (arrows).
irregular ingrowth of ciliated epithelium for a distance of 3 to 7 mm on both sides of the neotracheal segment. The central part of the neotrachea was covered with squamous epithelium. In four of nine long-term experiments the silicone rubber tube could be extracted 17 to 26 weeks after tracheal replacement. In two animals the Prolene suture cut through the tube, which was spontaneously dislocated toward the upper airway. This was observed in a clinically established stridor. The silicone rubber tube was immediately extracted without any effort by means of a tracheoscope. Shrinkage of the neotrachea segment was observed to a length of 4.2, 4.5, 4.5, and 4.6 em compared to the original distance of 5 em. In further tracheoscopic measurements the length of the neotracheal segment was the same and no further shrinkage occurred. The remaining Prolene suture served as a marker between the trachea and neotrachea(Fig. 6). Endoscopic evaluation of these four animals established macroscopially the absence of a margin at the transition of trachea and neotrachea 5 weeks, 10 weeks, 5 months, and 7 months after the removal of the stenting silicone rubber tube. The transparent cartilage strips were in an irregular position but not dislocated. Every part of them was covered with a fine network of vessels with vascularization originating in the intercartilaginous areas, where the presence of main vessels could be established macroscopically (Fig. 6). A subepithelial network of capillaries branched out from these vessels. Light microscopic studies of epithelial tissue from the entire epithelium proved the presence of ciliated epithelium in these
four animals. Transmission electron microscopic results confirmed the light microscopic findings (Fig. 7). With reference to samples from the native trachea, the quantity of cilia in epithelial cells of the neotrachea was reduced to 50%. However, the cilia were arranged in a regular order, and the tubules of the cilia were disposed according to the physiologic principle of order, 9 X 2 + 2. The central pair of the tubules was also placed in the correct local order, which indicates normal function of the cilia. The organs of the cells, because of their number of basal structure of tubules and their marked reticulum, indicate accelerated and intensified metabolic activity. From all these micromorphologic criteria of a normal ciliated epithelial cell we may deduce physiologic functioning. In two animals the ink test was performed 4 months after extraction of the silicone rubber tube to check mucociliary clearance. After ink particles had been blown in, proper transport in spirals of the marker to the upper airway could be observed. Transport speed equaled 18 to 21 mm/rnin (Fig. 6). The four animals are still alive and in excellent health after extraction of the stenting tube without any sign of tracheomalacia or stenosis. Discussion Endogenous tissue may be combined with foreign material in tracheal replacement. Roemer' was successful in some cases in bridging larger continuous defects of the trachea in dogs by using membrane from the small intestine combined with wire spirals. The conclusion from this use of tracheal isografts and homografts was that grafts over 3 em long were not feasible because of
Volume 94 Number 2 August 1987
Circumferential tracheal replacement
17 9
Fig. 7. Transmission electron micrograph of a biopsy specimen from the mucosa of the neotrachea 6 weeks after extraction of the silicone rubber tube. There were two ciliated epithelial cells. Longitudinal and cross-sections as well as the basal structure of the cilia were studied.
poor nutrition.' Drettner and Lindholm' followed the fate of a free composite graft from the nasal septum implanted in an experimentally created fenestrated defect of the cervical trachea in dogs. The object was to replace the trachea by tissue which was as similar as possible, that is, having mucous membrane for lining and cartilage as support. However, no remaining grafted cartilage was found by macroscopic examination 12 months after transplantation. The septal cartilage had been replaced by a layer of connective tissue. Flemming and Hemmerich' tested the suitability of a composite skin-cartilage graft taken from the auricle for partial tracheal defects in rabbits. Cartilage maintained its vitality, but there was also a series of sections showing transplanted squamous epithelium throughout, and in some cases the whole lumen was lined by respiratory epithelium. Botta and Meyer? have developed a solution for reconstruction of long tracheal segments. The procedure comprises a homograft cartilaginous support specially treated beforehand, a vascular pedicle the same length as the neotrachea, and mucosal cover. Even when porous tracheal prostheses were used, the lining of the lumen with ciliated epithelium did not succeed at full length." Of great importance for the method described in this article was the report by Poticha and Lewis? on excellent results achieved with steel mesh covered with autoplastic fibrocartilaginous
tissue used as tracheal replacement. Some inspiration was taken from Montgomery'? and Cooper and associates, II i.e., the treatment of instability of the trachea by means of aT-tube. Our experimental technique offers tracheal replacement with anatomical reconstruction and excellent blood supply along the whole segment of the neotrachea, right into the subepithelial layer, as a prerequisite for a functioning epithelium in the lumen. This is possible only if long-term incorporation of foreign material is avoided. Polyglactin seemed to us suitable for the production of sewing rings as it is absorbed without any reaction within 70 days. That means that 70 days at the latest after cartilage transplantation, no foreign body is present in the neotracheal wall and the repair process is not impeded. Ingrowth of the ciliated epithelium occurred when the sewing rings were absorbed. Although the strengthening process of the intercartilaginous bridges had not been completed yet, as we could see, epithelial migration had already progressed as far as the wall of the neotrachea permitted. This is the only way to avoid the appearance of stenosis or granulation tissue after extraction of the silicone rubber tube. The vitality of the transplants is a prior condition of the required stability. Vascularization of the neotracheal wall was a basic requirement for the transplants as well as for the epithelium. Blood vessels originated from the
The Journal of Thoracic and Cardiovascular Surgery
180 Eckersberger, Moritz. Wolner
mediastinal tissue as far as the transplant layer. There the vessels branched off and Provided a network for supply on the perichondrial side of the transplants. On the cutting surface of the transplants no connection of the vessels could be observed, even after the appearance of a tender pseudoperichondrium, What seems particularly significant to us is that the blood vessels from the mediastinum bypassed the transplantsconnecting to the subepithelial layer with main vessels and a diameter of 180 ~m in the subepithelial network. This type of blood distribution could even be seen macroscopically with an endoscope. We are thus dealing with parallel blood supply of the neotracheal wall and the epithelium. Compared to other techniques, ours succeeds as a one-time procedure overan observation period of up to 7 months with excellent health of the animals involved. We believe that a high rate of long-term success is possible in further attempts relevant to a clinical application of this technique if some points are noticed: 1. The temporary prosthesis has to be 3 mm smaller in diameter than the trachea. 2. The neotracheal wall must be conducted with cartilage strips. 3. The perichondrium of the strips has to be positionedadjacent to the mediastinal tissue for the nutrition for the transplants. 4. The stentingsilicone tube has to be left in placefor a minimum of 4' months. REFERENCES 1. Neville WE, Bolanowski PJP, Soltanzadeh H. Prosthetic reconstruction of the trachea and carina. J THORAC CARDIOVASC SURG 1976;72:525-38. 2. Duncan MJ, Thomson HG, Mancer JFJ(. Free cartilage grafts. the role of perichondrium. Plast Reconstr Surg 1984;73:916-233. Roemer K. Diinndarm- serosa-muscularis bezogene V2A-Drahtspiralen als Ersatz fur komplette Segmente des Tracheobronchialbaumes im Tierversuch. Langenbecks Arch KIin Chir 1961;298:781-95. 4. Scholzel E, Petropuolos P, Spycher M, Uhlschmid G. Die Revitalisierung des bovinen Xenografts als Trachealersatz beim Hund. Thoraxchirurgie 1978;26:172-6. 5. Dretter B, Lindholm CEo Experimental tracheal reconstruction with composite graft from the nasal septum. . Acta Otolaryngol Seand 1970;70:401-7. 6. Flemming I, Hommerich K. Tierexperimentelle Untersuchung zur Rekonstruktion der vorderen Trachealwand bei begrenzten Luftrohrenverengungen, Z Laryngol Rhinol 1968;47:336-41. 7. Botta Y, Meyer R. Reconstruction experimentale de la . trachee par microchirurgie. Praxis 1978;43:1588-92. 8. Nelson RJ, Goldberg L, White AR, Shors E, Hirose F. Neovascularity of a tracheal prosthesis/tissue complex. J THORAC CARDIOVASC SURG 1983;86:800-8.
9. Poticha SMF, Lewis FJ. Experimental replacement of the trachea. J THORAC CARDIOVASC SURG 1966;52:61-7. 10. Montgomery WW. Silicone tracheal 'l-tube, Ann Otolol Rhinol Laryngol 1974;83:71-8. 11. Cooper JD, Todd RJT, lives R, Pearson FG. Use of the silicone tracheal T-tube for the management of complex tracheal injuries. J THORAC CARDIOVASC SURG 1981; 82:559-68.
Discussion DR. HERMES C. GRILLO Boston, Mass.
The authors address one of the major remaining problems in tracheal reconstruction. Subtotal tracheal replacement is seldom necessary. However, when it is needed, there is not yet a truly adequate way to handle all the ramifications: that is, replacement of a large segment of trachea with a reconstruction that will really become an intimate part of the patient and therefore eliminate the serious complications that happen with plastic replacements. In this category of tracheal replacement-use of the subject's own tissues either with or without temporary stenting to create a stable tube--epithelialization has usually been attained by subsequent grafting with buccal mucosa or skin. The reason these techniques have never come into clinical use is that an unacceptable percentage will not succeed because of the complexity of the methods. The technique presented has the appeal of simplicity. However, in prior experiments in this category, where one has depended on epithelium growing in to cover. a long bed of connective tissue, total coverage has not been achieved in a large number of animals. In wound healing epithelial migration usually travels a certain distance and then stops. I may have missed the numbers. I would like to know from the author in what percentage of these rather lengthy segments was complete epithelialization achieved? If it was achieved in a large number, I think this could be an extraordinarily interesting and promising avenue to follow. . DR.ECKERSBERGER(a~m~
Thank you, Dr. Grillo, for your remarks. We now have an observation period of up to 7 months in replacement of the thoracic trachea and there has been no sign of stenosis, with physiologic function of the epithelium. It is necessary for the diameter of the temporary prosthesis, especially the stenting tube, to be 2 to 3 mm smaller than the diameter of the native trachea. Due to this fact, after absorption of the sewing rings, there is a split between the stenting tube and the tracheal wall which stops the ingrowth of epithelium. If there is no migration of epithelium, granulation occurs and stenosis in the neotracheal segment develops. The absence of migration of the epithelium is shown in a fold of the epithelial layer at the end of the stenting silicon rubber tube during the whole period until the tube is extracted. I would like to report the results after I or 2 more years of observing the animals.
THoRAc CARDIOVASC SURG
1987;94:175-80
Circumferential tracheal replacement with costal cartilage Long-termincorporation of foreign material or tissue in circumferential tracheal replacement will lead to progressive growth of granulation tissue, provoking either airway stenosis or a reduction of subepithe6al blood supply and thereby preventing the appearance of functioning ciliated epithelium in the replaced segment In experience with dogs, a 5 cm length of the thoracic trachea was replaced circumferentially with fresh autogenous untreated circularly positioned cartilage-perichrondrlum strips. During the period of strengthening of this neotracheal wall, a temporary tracheal prosthesis made of tubular siliconerubber withabsorbablesewing rings of polyglactin910 placed 3 mm from the end of the tube servedas a tracheal replacement Six months after the cartilage transplantation, the neotracheal wall had stabilized sufficiently for the siliconerubber tube to be extracted with an endoscope. Four weeks after extraction of the silicone rubber tube the neotracheal segment was completely covered with ciliated epithelium over a thin subepithelial, weD-vascularized layer. Subepithe6al vessels had a diameter of 180 ~m. They were a continuation of the intercartilaginous main vessels of the neotracheal wall. The presenceof normal cilia on the epithelium was proved through transmission electron microscopy. Even the tubules of the cilia were arranged in the right order. In the ink test, movement of the transport marker across the neotracheal segmentat a speed of 18 to 21 mm/min was proof of mucociliary clearance. In a process of migration starting from the margin of the trachea, the ciliated epithelium pervaded and replaced the preexisting temporary one-layer stratified squamous epithelium. This completely new technique of circumferential tracheal replacement with autogenous cartilage, avoiding permanent incorporation of foreign material, succeeds witbinthe observation period of up to 7 months.
Franz Eckersberger, M.D. (by invitation), Erich Moritz, M.D. (by invitation), and Ernst Wolner, M.D. (by invitation), Vienna, Austria Sponsored by Thomas W. Shields, M.D., Chicago, Ill.
EreqUisites for the clinical application of a technique for long-term replacement of a segment of trachea are the mechanical stability of the neotrachea and the complete covering of the lumen with ciliated epithelium in the absence of granulation tissue. We have tried to develop a circumferential tracheal replacement by transplanting autogenous fresh untreated cartilage for the production of a neotrachea to avoid permanent incorporation of foreign material. While the neotrachea consisting of transplanted cartilaginous tissue was allowed to strengthen, a silicone rubber prosthesis was implanted. Becauseabsorbable sewing rings were used, this prostheFrom the II. Surgical Clinic, University of Vienna, Vienna, Austria. Read in part at the Sixty-sixth Annual Meeting of The American Association for Thoracic Surgery, New York, N. Y., April 28-30, 1986. Address for reprints: Franz Eckersberger, M.D., II. Surgical Clinic, University of Vienna, Spitalgasse 23, A-1090 Vienna, Austria.
sis transformed itself into a tubular stent within the neotrachea, which could be extracted endoscopically. A$ there are no publications describing the transplantation of a cartilage-perichondrium strip into the mediastinum, experience had to be gathered from previous experiments to work out the optimum device for transplantation in relation to the required stability and to define the position of the perichondrial side of the transplant that would achieve long-term vitality of the cartilaginous tissue.
Material and methods A tracheal prosthesis 5.6 em long was fabricated from a silicone rubber tube* with a wall thickness of 1.5 mm (Fig. 1). The sewing rings were sutured 3 mm from the end of the tube with a polyglactin 910 running suture. *Silastic sheeting; reinforced, medical-grade silicone rubber; Dow Corning Corporation, Midland, Mich.
175
176 Eckersberger, Moritz, Wainer
Fig. 1. Temporary tracheal prosthesis with subterminal sewing rings that consisted of absorbable polyglaetin 910. Within 70 days the prosthesis is changing to a tube of silicone rubber stenting the neotracheal wall with the possibility of being telescoped into the native trachea.
These rings consisted of three circular layers of a polyglactin 910 band. * After right thoracotomy and resection of 5 em of the thoracic trachea, this tracheal prosthesis was interposed in mongrel dogs weighing 26 to 34 kg. The operation, performed with standard anesthesia, was done according to the method described by Neville, Bolanowski, and Soltanzadeh.' Free fresh autotransplant tissue made of costal cartilage was positioned circumferentially around this prosthesis and the ends of the strips were connected with an absorbable 4-0 polyglactin suture to produce a ring of strips around the prosthesis (Fig. 2, A and B). These transplants were taken immediately before transplantation from the partially resected cartilaginous part of the seventh and eighth ribs on the right side near the sternum after preparation with a scalpel (Fig. 3). The time between preparation and transplantation was less than 1 hour in all cases. The mediastinal pleura around these transplants was reconstructed so that it would close. Thus the mediastinal tissue was wrapped about the transplants for nutrition. Cartilage-perichondrium chips (3 mm in width, 1.5 em in length), cartilage-perichondrium strips (3 mm in width, 8 em in length), and cartilage-bone chips (3 mm in width, 2 em in length) were used for transplantation. The transplants were between 2 and 3 mm thick. The perichondrium was positioned partly about the prosthe*Vicryl band, 3 mm; Ethicon, Inc., Somerville, N. J.
The Journal of Thoracic and Cardiovascular Surgery
Fig. 2. A, Fresh free autotransplants of cartilage-perichondrium stripswereusedin long-term experiments. Theycovered the implanted tracheal prosthesis in circumferential rings. The perichondrial side of the transplants was positioned on the outer, cutting surface of the prosthesis. B, The ends of the strips were connected with an absorbable 4-0 polyglactin suture producing a ring of strips around the prosthesis. sis and partly adjacent to the nutritive mediastinal tissue. For every experiment four different sizes of prosthesis with diameters of 15,17,19, and 21 mm were prepared to ensure that the implanted prosthesis would be perfectly fitted to the diameter of the trachea. A 3-0 Prolene suture secured the prosthesis at the cranial margin of resection of the trachea to prevent dislocation of the silicone rubber tube after absorption of the sewing rings. The animals were divided into two groups. Group I. Five animals were electively put to death 6 to 9 weeks after cartilage transplantation to assess the vitality of the transplants. Vitality was judged with the use of a light microscope' and delineated in percent of specimens as a means of comparison. Group II. Group II comprised nine dogs used for long-term experiments. Stabilization and vascularization of the neotracheal wall were examined as was the epithelial covering of the lumen after extraction of the silicone rubber tube. Bronchoscopic examinations were performed regularly. Before extraction of the silicone rubber tube with a biopsy forceps, the Prolene suture was cut through with an endoscopy scissors. For extraction, the silicone rubber tube was telescoped in the rigid bronchoscope and the two were removed together. Transmission electron microscopic examination of epithelial biopsy tissue followed 4 weeks, 2 months, and 4 months after extraction of the silicone rubber tube. The function of mucociliary
Volume 94 Number 2 August 1987
Fig. 3. Transplant strips were preparated with the scalpel from the cartilaginous part of two ribs. The bony central part was not used in long-term experiments. In this way, each transplant had a cutting surface side and a perichondrial side.
Circumferential tracheal replacement
17 7
Fig. 4. After the mediastinal pleura was split, the mediastinal tissue was divided so that the main vessels were saved for a well-vascularized bed for the transplants.
clearance was tested by blowing dry ink particles (diameter 20 to 80 JLm) into the region of tracheal bifurcation of the anesthetized, spontaneously breathing animal followed by documentation of the transport speed of the marker with endoscopic photographs taken at intervals of 10 seconds. All animals received humane care in compliance with the Austrian "Law of Animal Experiments."
Results
Group I. Cartilage-bone transplants retained the least vitality. The bony part of the transplants had devitalized areas at regular intervals. The chip transplants retained the highest vitality: Dislocation of the chips was observed, however, which means the stability required for the trachea did not seem ensured. Those transplant strips whose perichondrial surface had been transplanted adjacent to the mediastinal tissue showed greater vitality than those cartilage-perichondrium strips that had been transplanted with the perichondrium over the tracheal prosthesis and the cutting surface of the preparation positioned adjacent to the mediastinal tissue (Fig. 4). Group II. In further long-term experiments based on this knowledge,only cartilage-perichondrium strips were used with perichondrium positioned adjacent to the mediastinal tissue; the cutting surface of the scalpel was thus superimposed on the tracheal prosthesis to the silicone rubber tube. We have also observed that the diameter of the tracheal prosthesis must be 2 to 3 mm smaller than the diameter of the trachea, so as to leave a split for invagination between the trachea and silicone rubber tube. The latter permitted telescope-like invagination of the tube into the trachea from the thirty-fifth day after tracheal replacement onward. This split for invagination enabled the epithelium to migrate from the
Fig. 5. Photographs taken through a Storz telescope 9 weeks after implantation of a prosthesis.The outer diameter was the same as that of the native trachea. As a result, no telescoping and migration of the epithelium was possible.A fold of mucosa was seen at the end of the silicone rubber tube.
margin of the native trachea while the silicone rubber tube was still in its position. If the diameter of the tracheal prosthesis was equal to that of the trachea, no epithelial migration from the margin of the trachea into the surface of the neotrachea could be observed. On the contrary, a fold of mucosa (Fig. 5) appeared at the margin of the trachea disrupting the ciliated epithelium at the margin of the neotrachea. The latter was homogeneously lined with substituting squamous epithelium, as we have seen in three dogs. The same occurred in two dogs when the prosthesis was smaller in diameter than the native trachea but the wall of the neotrachea was devitalized. Subtotal airway stenosis occurred in 1 to 12 days after extraction of the silicone rubber tube because of granulation tissue and malacia of the neotracheal segment. There was only an
The Journal of
1 7 8 Eckersberger, Moritz, Wolner
Thoracic and Cardiovascular Surgery
Fig. 6. Photographs of the neotracheal segment 4 months after extraction of the silicone rubber tube during the ink test to check the mucociliary clearance function. Spiral transportation form of the dry marker particles is observed even in the neotracheal segment. Time interval between left and right is 30 seconds. During this time, a test marker was transported 11 mm in the cranial direction (arrows).
irregular ingrowth of ciliated epithelium for a distance of 3 to 7 mm on both sides of the neotracheal segment. The central part of the neotrachea was covered with squamous epithelium. In four of nine long-term experiments the silicone rubber tube could be extracted 17 to 26 weeks after tracheal replacement. In two animals the Prolene suture cut through the tube, which was spontaneously dislocated toward the upper airway. This was observed in a clinically established stridor. The silicone rubber tube was immediately extracted without any effort by means of a tracheoscope. Shrinkage of the neotrachea segment was observed to a length of 4.2, 4.5, 4.5, and 4.6 em compared to the original distance of 5 em. In further tracheoscopic measurements the length of the neotracheal segment was the same and no further shrinkage occurred. The remaining Prolene suture served as a marker between the trachea and neotrachea(Fig. 6). Endoscopic evaluation of these four animals established macroscopially the absence of a margin at the transition of trachea and neotrachea 5 weeks, 10 weeks, 5 months, and 7 months after the removal of the stenting silicone rubber tube. The transparent cartilage strips were in an irregular position but not dislocated. Every part of them was covered with a fine network of vessels with vascularization originating in the intercartilaginous areas, where the presence of main vessels could be established macroscopically (Fig. 6). A subepithelial network of capillaries branched out from these vessels. Light microscopic studies of epithelial tissue from the entire epithelium proved the presence of ciliated epithelium in these
four animals. Transmission electron microscopic results confirmed the light microscopic findings (Fig. 7). With reference to samples from the native trachea, the quantity of cilia in epithelial cells of the neotrachea was reduced to 50%. However, the cilia were arranged in a regular order, and the tubules of the cilia were disposed according to the physiologic principle of order, 9 X 2 + 2. The central pair of the tubules was also placed in the correct local order, which indicates normal function of the cilia. The organs of the cells, because of their number of basal structure of tubules and their marked reticulum, indicate accelerated and intensified metabolic activity. From all these micromorphologic criteria of a normal ciliated epithelial cell we may deduce physiologic functioning. In two animals the ink test was performed 4 months after extraction of the silicone rubber tube to check mucociliary clearance. After ink particles had been blown in, proper transport in spirals of the marker to the upper airway could be observed. Transport speed equaled 18 to 21 mm/rnin (Fig. 6). The four animals are still alive and in excellent health after extraction of the stenting tube without any sign of tracheomalacia or stenosis. Discussion Endogenous tissue may be combined with foreign material in tracheal replacement. Roemer' was successful in some cases in bridging larger continuous defects of the trachea in dogs by using membrane from the small intestine combined with wire spirals. The conclusion from this use of tracheal isografts and homografts was that grafts over 3 em long were not feasible because of
Volume 94 Number 2 August 1987
Circumferential tracheal replacement
17 9
Fig. 7. Transmission electron micrograph of a biopsy specimen from the mucosa of the neotrachea 6 weeks after extraction of the silicone rubber tube. There were two ciliated epithelial cells. Longitudinal and cross-sections as well as the basal structure of the cilia were studied.
poor nutrition.' Drettner and Lindholm' followed the fate of a free composite graft from the nasal septum implanted in an experimentally created fenestrated defect of the cervical trachea in dogs. The object was to replace the trachea by tissue which was as similar as possible, that is, having mucous membrane for lining and cartilage as support. However, no remaining grafted cartilage was found by macroscopic examination 12 months after transplantation. The septal cartilage had been replaced by a layer of connective tissue. Flemming and Hemmerich' tested the suitability of a composite skin-cartilage graft taken from the auricle for partial tracheal defects in rabbits. Cartilage maintained its vitality, but there was also a series of sections showing transplanted squamous epithelium throughout, and in some cases the whole lumen was lined by respiratory epithelium. Botta and Meyer? have developed a solution for reconstruction of long tracheal segments. The procedure comprises a homograft cartilaginous support specially treated beforehand, a vascular pedicle the same length as the neotrachea, and mucosal cover. Even when porous tracheal prostheses were used, the lining of the lumen with ciliated epithelium did not succeed at full length." Of great importance for the method described in this article was the report by Poticha and Lewis? on excellent results achieved with steel mesh covered with autoplastic fibrocartilaginous
tissue used as tracheal replacement. Some inspiration was taken from Montgomery'? and Cooper and associates, II i.e., the treatment of instability of the trachea by means of aT-tube. Our experimental technique offers tracheal replacement with anatomical reconstruction and excellent blood supply along the whole segment of the neotrachea, right into the subepithelial layer, as a prerequisite for a functioning epithelium in the lumen. This is possible only if long-term incorporation of foreign material is avoided. Polyglactin seemed to us suitable for the production of sewing rings as it is absorbed without any reaction within 70 days. That means that 70 days at the latest after cartilage transplantation, no foreign body is present in the neotracheal wall and the repair process is not impeded. Ingrowth of the ciliated epithelium occurred when the sewing rings were absorbed. Although the strengthening process of the intercartilaginous bridges had not been completed yet, as we could see, epithelial migration had already progressed as far as the wall of the neotrachea permitted. This is the only way to avoid the appearance of stenosis or granulation tissue after extraction of the silicone rubber tube. The vitality of the transplants is a prior condition of the required stability. Vascularization of the neotracheal wall was a basic requirement for the transplants as well as for the epithelium. Blood vessels originated from the
The Journal of Thoracic and Cardiovascular Surgery
180 Eckersberger, Moritz. Wolner
mediastinal tissue as far as the transplant layer. There the vessels branched off and Provided a network for supply on the perichondrial side of the transplants. On the cutting surface of the transplants no connection of the vessels could be observed, even after the appearance of a tender pseudoperichondrium, What seems particularly significant to us is that the blood vessels from the mediastinum bypassed the transplantsconnecting to the subepithelial layer with main vessels and a diameter of 180 ~m in the subepithelial network. This type of blood distribution could even be seen macroscopically with an endoscope. We are thus dealing with parallel blood supply of the neotracheal wall and the epithelium. Compared to other techniques, ours succeeds as a one-time procedure overan observation period of up to 7 months with excellent health of the animals involved. We believe that a high rate of long-term success is possible in further attempts relevant to a clinical application of this technique if some points are noticed: 1. The temporary prosthesis has to be 3 mm smaller in diameter than the trachea. 2. The neotracheal wall must be conducted with cartilage strips. 3. The perichondrium of the strips has to be positionedadjacent to the mediastinal tissue for the nutrition for the transplants. 4. The stentingsilicone tube has to be left in placefor a minimum of 4' months. REFERENCES 1. Neville WE, Bolanowski PJP, Soltanzadeh H. Prosthetic reconstruction of the trachea and carina. J THORAC CARDIOVASC SURG 1976;72:525-38. 2. Duncan MJ, Thomson HG, Mancer JFJ(. Free cartilage grafts. the role of perichondrium. Plast Reconstr Surg 1984;73:916-233. Roemer K. Diinndarm- serosa-muscularis bezogene V2A-Drahtspiralen als Ersatz fur komplette Segmente des Tracheobronchialbaumes im Tierversuch. Langenbecks Arch KIin Chir 1961;298:781-95. 4. Scholzel E, Petropuolos P, Spycher M, Uhlschmid G. Die Revitalisierung des bovinen Xenografts als Trachealersatz beim Hund. Thoraxchirurgie 1978;26:172-6. 5. Dretter B, Lindholm CEo Experimental tracheal reconstruction with composite graft from the nasal septum. . Acta Otolaryngol Seand 1970;70:401-7. 6. Flemming I, Hommerich K. Tierexperimentelle Untersuchung zur Rekonstruktion der vorderen Trachealwand bei begrenzten Luftrohrenverengungen, Z Laryngol Rhinol 1968;47:336-41. 7. Botta Y, Meyer R. Reconstruction experimentale de la . trachee par microchirurgie. Praxis 1978;43:1588-92. 8. Nelson RJ, Goldberg L, White AR, Shors E, Hirose F. Neovascularity of a tracheal prosthesis/tissue complex. J THORAC CARDIOVASC SURG 1983;86:800-8.
9. Poticha SMF, Lewis FJ. Experimental replacement of the trachea. J THORAC CARDIOVASC SURG 1966;52:61-7. 10. Montgomery WW. Silicone tracheal 'l-tube, Ann Otolol Rhinol Laryngol 1974;83:71-8. 11. Cooper JD, Todd RJT, lives R, Pearson FG. Use of the silicone tracheal T-tube for the management of complex tracheal injuries. J THORAC CARDIOVASC SURG 1981; 82:559-68.
Discussion DR. HERMES C. GRILLO Boston, Mass.
The authors address one of the major remaining problems in tracheal reconstruction. Subtotal tracheal replacement is seldom necessary. However, when it is needed, there is not yet a truly adequate way to handle all the ramifications: that is, replacement of a large segment of trachea with a reconstruction that will really become an intimate part of the patient and therefore eliminate the serious complications that happen with plastic replacements. In this category of tracheal replacement-use of the subject's own tissues either with or without temporary stenting to create a stable tube--epithelialization has usually been attained by subsequent grafting with buccal mucosa or skin. The reason these techniques have never come into clinical use is that an unacceptable percentage will not succeed because of the complexity of the methods. The technique presented has the appeal of simplicity. However, in prior experiments in this category, where one has depended on epithelium growing in to cover. a long bed of connective tissue, total coverage has not been achieved in a large number of animals. In wound healing epithelial migration usually travels a certain distance and then stops. I may have missed the numbers. I would like to know from the author in what percentage of these rather lengthy segments was complete epithelialization achieved? If it was achieved in a large number, I think this could be an extraordinarily interesting and promising avenue to follow. . DR.ECKERSBERGER(a~m~
Thank you, Dr. Grillo, for your remarks. We now have an observation period of up to 7 months in replacement of the thoracic trachea and there has been no sign of stenosis, with physiologic function of the epithelium. It is necessary for the diameter of the temporary prosthesis, especially the stenting tube, to be 2 to 3 mm smaller than the diameter of the native trachea. Due to this fact, after absorption of the sewing rings, there is a split between the stenting tube and the tracheal wall which stops the ingrowth of epithelium. If there is no migration of epithelium, granulation occurs and stenosis in the neotracheal segment develops. The absence of migration of the epithelium is shown in a fold of the epithelial layer at the end of the stenting silicon rubber tube during the whole period until the tube is extracted. I would like to report the results after I or 2 more years of observing the animals.