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Ann Thorac Surg 2000;70:1886-1890
© 2000 The Society of Thoracic Surgeons


Original article: general thoracic

Experimental tracheal reconstruction with a rotated right stem bronchus

Hiroaki Osada, MDa, Koji Kojima, MDa

a Department of Surgery, Division of Chest Surgery, St. Marianna University School of Medicine, Kawasaki, Japan

Accepted for publication May 3, 2000.

Address reprint requests to Dr Osada, Department of Surgery, Division of Chest Surgery, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae-ku, Kawasaki, Japan 216-8511
e-mail: h2osada{at}marianna-u.ac.jp


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. To reconstruct a longer tracheal defect, a safe method other than end-to-end anastomosis is necessary.

Methods. Nine mongrel dogs underwent right thoracotomy. The lobes of the right lung other than the apical lobe were resected, keeping the bronchi in place to be manipulated to extend the right stem bronchial conduit. The trachea was resected for a 10-cartilage-ring length. The modified right stem bronchus was then brought into the mediastinum by rotation in the frontal plane. An end-to-end anastomosis was made. The right apical lobe, once separated, was then reanastomosed end-to-side. Ciliary transport was studied.

Results. Eight of the 9 dogs tolerated the surgical procedure well, and the reanastomosed right apical lobe remained well expanded for 1 year or more postoperatively. The inverted segment did not show any cranial ciliary transport movement.

Conclusions. A large tracheal defect more than 10 rings in length can be reconstructed using a rotated right stem bronchus with the right apical lobe reanastomosed. The inverted bronchial segment loses its cranial ciliary transport movement.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Tracheal defects in excess of half the entire length need to be reconstructed by a method other than end-to-end anastomosis, because the latter frequently results in disastrous complications. An artificial trachea seems to be the choice in this situation, but its use in clinical practice still needs to be refined. Using dogs we have tested a hypothesis that a stem bronchus may be utilized safely to reconstruct a long tracheal defect with acceptable loss of the pulmonary parenchyma.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Nine mongrel dogs weighing 13 to 20 kg were anesthetized with intravenous pentobarbital sodium (25 mg/kg) and then intubated endotracheally for inhalation anesthesia with nitrous oxide through an anesthetic instrument (Mera AP-50 Senko Ika Kogyo, Tokyo, Japan) under controlled mechanical ventilation (Mera/ADV-1000MK II, Tokyo, Japan). Muscle relaxation was obtained by an intravenous bolus injection of 0.08 mg/kg pancuronium bromide followed by additional administration as needed.

With each dog in left lateral position a right thoracotomy was carried out, where the thoracic cavity was entered through the fourth intercostal space. The cardiac, intermedius, and diaphragmatic lobes were resected, preserving the intermedius and diaphragmatic lobe bronchi as far as possible. The cut end of the cardiac lobe bronchus was closed with 5-0 polyglycolic acid sutures. A pair of vascular clamps was applied to the right stem bronchus to prevent air leakage. The intermedius and diaphragmatic lobe bronchi were cut longitudinally, including the spur between them. The bronchi were then modified with running 5-0 polyglycolic acid suture to have an extension of the right stem bronchus in the form of a single conduit with a single distal stoma. Then the right apical lobe bronchus was severed at the point closest to the trachea without compromising the pulmonary artery and vein belonging to the apical lobe. The proximal cut end was closed immediately with a running 5-0 polyglycolic acid suture (Fig 1A).




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Fig 1. (A) Lobes of the right lung other than the apical lobe were resected. However, the bronchi of the diaphragmatic and intermedius lobes were left in place and then manipulated to create an extension of the right stem bronchus to form a single conduit by cutting the lobar bronchi longitudinally and then suturing. A pair of vascular clamps was applied to the right stem bronchus to prevent air leakage during the procedure. The apical lobe bronchus was then severed, and the proximal end was closed with sutures. (B) A segment of the mediastinal trachea 10 cartilage rings in length was resected, and the distal end was closed with an autostapler. Another endotracheal tube was inserted retrogradely through the right stem bronchus to ventilate the left lung. Subsequently, the entire right stem bronchus was rotated (arrow) in the frontal plane with the main carina as the center of rotation. (C) The original distal end of the extended right stem bronchus was anastomosed end-to-end to the proximal end of the trachea. A hole was then made in the lateral wall of the rotated stem bronchus, to which the right apical lobe bronchus was anastomosed.

 
A short-cuffed endotracheal tube (FR-31 DF-cuffed long type, Fuji System Corp, Tokyo, Japan) was inserted retrogradely into the right stem bronchus up to the carina after removal of the occluding clamp. The mediastinal trachea was then segmentally resected for a 10-cartilage-ring length, and the distal cut end was closed with an autostapler (Autosuture TA-30, U.S. Surgical Corp, Norwalk, CT) (Fig 1B).

The right stem bronchus thus manipulated was subsequently rotated cranially in the frontal plane with the endotracheal tube in place, with the main carina as the center of rotation. The carina was mobilized by gentle blunt dissection applied by a fingertip down to the midportion of the left main bronchus, whereas the tracheobronchial ligament was left intact to avoid injury of the bronchial arteries. The anatomically distal end of the right stem bronchus was then brought into the mediastinum to face the proximal cut end of the trachea, where an end-to-end anastomosis was made with a couple of running 4-0 polyglycolic acid sutures. The ventilation pathway was then switched back to the per orally inserted endotracheal tube. A side hole was made in the right lateral (originally medial) wall of the right main bronchus to fit the size of the right apical lobe bronchial stump. The right apical lobe bronchus was sutured to this hole in an end-to-side fashion with a couple of running 5-0 polyglycolic acid sutures. The surgeon’s fingertip was applied intermittently to occlude the hole during suturing to assist the ventilation of the left lung (Fig 1C).

Each dog was extubated after recovery from anesthesia and left to recover. Doxycycline (100 mg) was administered intramuscularly immediately after operation and on days 1 and 2. Per oral erythromycin (400 mg/day) was given mixed in the diets for 5 days thereafter.

Two to 3 months after operation a chest roentgenogram was obtained under intravenous anesthesia with pentobarbital (Electrical Diagrams for X-ray Radiographic System for Small Animal Clinics Model VPX-20, Toshiba Medical, Ayase, Japan). Bronchoscopic examinations were performed routinely 4 to 5 months after operation using an Olympus BF-10 bronchoscope (Olympus, Japan) and were repeated after 1 year, when the stomata were photographed.

To examine the ciliary transport in the inverted segment of the bronchus, measurement of the speed of ciliary transport was attempted in dogs 6 to 9 using 2 other normal dogs as controls. Barium sulfate was diluted just sufficiently to allow it to remain on the mucosal surface in the form of droplets when delivered through the utility channel of the bronchoscope, with the dogs in a supine position under intravenous pentobarbital anesthesia. One milliliter of the prepared dye was spread in a patchy fashion on the mucosal surface of one of the dorsal bronchi in the left lung, the inverted stem bronchus, and the cervical trachea, respectively. Under fluoroscopy the cranial movement of each patch of the dye was videotaped and its speed measured in millimeters per minute. The obtained data were compared by t test and p less than 0.05 was considered significant.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
The postoperative course of the dogs is summarized in Table 1. Postoperative air leakage did not take place in any of the dogs, but 1 of the 9 dogs died shortly after operation due to continuous airway bleeding. The other 8 dogs tolerated the surgical procedure well and survived for between 10 months and 2 years 3 months. Examination of chest roentgenograms showed a well-expanded remaining right apical lobe in each dog (Fig 2), and bronchoscopy revealed almost uniformly well-patent tracheobronchial and bronchobronchial anastomoses (Fig 3), although a few anastomoses showed slight stenosis or torsion. All 8 dogs remained well and active but were sacrificed for histologic examination of the anastomoses (Table 1). This revealed mostly smooth continuity of the bronchotracheal and bronchobronchial anastomoses without undue granuloma formation or deformity.


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Table 1. Postoperative Course of the Dogs Undergoing Tracheal Reconstruction Using a Rotated Right Stem Bronchus

 


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Fig 2. (Dog 4.) Plain chest x-ray film shows the well-patent right apical lobe 3 months after operation.

 


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Fig 3. (Dog 5.) Bronchoscopic views obtained 1 year after operation. (Right) Smooth mucosa at the site of anastomosis of the rotated right stem bronchus to the original trachea. (Left) Well-healed and well-patent anastomosis of the right apical lobe (to the right) and the left main bronchus (to the left) beyond the original main carina.

 
Ciliary transport speeds measured for each of the three divisions of the airway are listed in Table 2. In the experimental dogs the cervical trachea and the bronchi of the remaining left lung transported the dye with a speed comparable with that in the normal control dogs. However, the rotated portion of the stem bronchi showed zero ciliary transport during observation for 50 minutes. It was seen that the radiopaque dye placed on the bronchial mucosa in the left lung moved orally with time, but accumulated just on the line of the carina. In other words, the right main bronchus which had been placed in an inverted position after rotation could not transport the dye in a cranial direction, although the intact cervical trachea and the bronchi in the experimental dogs maintained normal transport ability.


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Table 2. Speed of Musocal Transport Observed by Dye Movement Under Fluoroscopya

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
In humans a tracheal defect longer than 5 to 6 cm—or more than 9 to 10 tracheal rings—is generally considered to be beyond the maximum length for safe resection and reanastomosis [1]. For reconstruction of such a long defect, methods other than end-to-end anastomosis are needed. Akl and associates [2] first reported experimental reconstruction of a tracheal defect using a rotated left main bronchus. They extended their work to employ the technique clinically, but their patient died shortly after operation [3]. In our laboratory, Yokote [4] reported an extended experiment in which the lobar bronchi were modified so as to become an extension of the left main bronchus as a conduit. Kurisu [5], also from our laboratory, reported a successful experiment conducted on the right side, where lobar bronchi were manufactured in a similar manner to form a single conduit to replace a long segmental defect of the trachea.

Total sacrifice of either the left or the right lung in our two series of experiments was considered to result in excessive loss of undiseased lung parenchyma, especially in pediatric patients. Therefore, we tried to preserve more of the lung parenchyma. Preservation of the right apical lobe proved amenable in the present series of experiments. During our work in this issue Murakami and colleagues [6] reported that a successful repair had been done experimentally in a similar way, with right lower lobes preserved. Our result is in accordance with theirs. This method of reconstructing long defects of the trachea can thus be considered applicable in a clinical situation.

In spite of multiple suture closures and anastomoses, postoperative air leakage was not found among the experimental dogs. One of the reasons for this was probably because we used running sutures for anastomoses. Although a running suture technique is not recommended from the viewpoint of preventing ischemia at the anastomotic margins, we used it simply because we had not encountered a problem with it in our preceding series of experiments [4, 5].

Another concern was the effect of this technique on ciliary transport, since no other previous reports had addressed this issue other than the one by Murakami and colleagues [6], wherein they reported cessation of the mucociliary transport in the inverted segment of the bronchus. Because we could not apply any radioactive material to the dogs in our laboratory, we had to employ some other method of measuring the speed of ciliary transport. Our results showed that ciliary motion was arrested for about 1 year after reversal of the right stem bronchus. The reason why ciliary motion in the inverted segment of the bronchus loses its original axiality remains to be studied.

In this regard, it is quite interesting to read a report [7] that even direct bronchial artery revascularization at the time of lung transplantation did not have any demonstrable influence on ciliary beat frequency, and that the abundance of ciliated epithelial cells was preserved in the bronchi of the transplanted lungs irrespective of bronchial artery revascularization. Another report [8] pays attention also to the possibility that denervation at the time of lung transplantation may relate to changes in rheologic characteristics of mucus which impair mucociliary clearance after transplantation. These reports state that ciliary function was more or less preserved after a variety of surgical interventions, most of which were with devascularization or denervation. Long-standing cessation of cranial ciliary transport in our dogs may well be related to the 180-degree inversion of the anatomical axis, which may have some disturbing effect on the direction of ciliary motion. However, it is noteworthy that the dogs that underwent the experimental operation did well without any airway clearing after the procedure, despite the impaired ciliary motion. Normal expectoration seemed to be sufficient for overcoming the defective ciliary motion. We again agree with Murakami and colleagues [6].

In applying this method clinically, we need to consider the anatomical differences in blood supply between dogs and humans. Miller and coworkers [9] and Notkovich [10] stated that dogs have a tracheobronchial blood supply almost identical to that in humans. Cantrell and Folse [11] reported that severing the airway at any site in dogs would retain a sufficient blood supply at either cut end as long as the inferior thyroid artery and the bronchial arteries in the region of the pulmonary hilum were preserved. These findings are compatible with our observation of uniformly active bleeding at each cut end of either the trachea or the bronchus during operation in our dogs.

The operative technique we used in this series of experiments, namely lateral thoracotomy and reanastomosis of the right apical lobe back in place, may have the edge on the median sternotomy with pneumonectomy that was used clinically by Akl and colleagues [3]. They suspected that the cause of death in their young patient was the mediastinal shift leading to kinking or twisting of the bronchus. Stability of the mediastinum seems like an important part of this procedure.

The length of the right stem bronchus in an average Japanese adult man is reported to be 5.2 cm [12]. This would be 5.5 to 6.0 cm after plastic manipulation to create an extension of the conduit. The diameter of the distal-most portion of the right stem bronchus is considered to be more than 50% that of the trachea [12]. The diameter of the stoma of the extended conduit of the right stem bronchus should then become much more than 50% that of the trachea after the manipulative combination of stomata of the lobar bronchi. The rotated right stem bronchus would thus be long enough and functionally compatible for reconstructing a defect longer than 50% of the entire tracheal length. By analogy, it may well be acceptable that in man the upper lobe can be reanastomosed to the stem bronchus inverted after resection of the middle and lower lobes. The initial distal end could be made up by sacrificing the superior segmental bronchus of the lower lobe and making a single stoma with both the basal bronchus and the middle lobe bronchus together. In clinical situations slight cervical flexion can easily lower the cranial end of the trachea down into the mediastinum at least 1.0 cm, then the trachea may be resected for at least 7.0 cm for safe reconstruction by this method.

The technique reported here should be considered in comparison with other methods of tracheal reconstruction. Allograft tracheal transplantation is the most exciting among the latter. Jacobs and associates [13] have recently reported North American as well as worldwide pediatric experience in tracheal allografts applied clinically, with encouraging short- to medium-term results. Use of cardiopulmonary bypass along with heparinization appears to be disadvantageous. A slide tracheoplasty has long been accepted in pediatric operations. Our method for reconstruction of a long tracheal defect reported here may well be considered an alternative in a clinical situation.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
We are deeply grateful to Ms Kayoko Tanaka for her expert technical assistance and preparation of the experiments.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Couraud L., Jougon J.B., Velly J.-F. Surgical treatment of nontumoral stenoses of the upper airway. Ann Thorac Surg 1995;60:250-260.[Abstract/Free Full Text]
  2. Akl B.F., Mittelman J., Smith D.E., Butler C. A new method of tracheal reconstruction. Ann Thorac Surg 1983;36:265-269.[Abstract]
  3. Akl B.F., Yabek S.M., Berman W., Jr Total tracheal reconstruction in a 3-month-old infant. J Thorac Cardiovasc Surg 1984;87:543-546.[Abstract]
  4. Yokote K. Reconstruction of the trachea with an extension of the reversed left main bronchus. An experimental study. J Jpn Assoc Chest Surg 1991;5:129-136.
  5. Kurisu S. Use of the reversed right central bronchi for reconstruction of the trachea. St Marianna Univ J 1990;18:580-585.
  6. Murakami S., Sato H., Uno Y., et al. Tracheal reconstruction after lower tracheal resection using the inverted right bronchus—an experimental study. Thorac Cardiovasc Surgeon 1993;41:335-339.[Medline]
  7. Nørgaard M.A., Andersen C.B., Pettersson G. Airway epithelium of transplanted lungs with and without direct bronchial artery revascularization. Eur J Cardiothorac Surg 1999;15:37-44.[Abstract/Free Full Text]
  8. Paul A., Marelli D., Shennib H., et al. Mucociliary function in autotransplanted, allotransplanted, and sleeve resected lungs. J Thorac Cardiovasc Surg 1989;98:523-528.[Abstract]
  9. Miller M.E., Christensen G.C., Evans H.E. Anatomy of the dog. Philadelphia: WB Saunders, 1964:726-739.
  10. Notkovich H. The anatomy of the bronchial arteries of the dog. J Thorac Surg 1957;33:242-253.
  11. Cantrell J.R., Folse J.R. The repair of circumferential defects of the trachea by direct anastomosis: experimental evaluation. J Thorac Cardiovasc Surg 1961;42:589-598.
  12. Minoshima T. List of numerical data of normal Japanese body. Tokyo: Gihohdoh, 1967:278-280.
  13. Jacobs J.P., Quintessenza J.A., Andrews T., et al. Tracheal allograft reconstruction: the total North American and worldwide pediatric experiences. Ann Thorac Surg 1999;68:1043-1052.[Abstract/Free Full Text]



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