- Email: [email protected]
Reversed free periosteal grafting of extensive tracheal defects in dogs
Reversed Free Periosteal Grafting of Extensive Tracheal Defects in Dogs By Christopher Moutsouris, Panayotis Karayannakos, Michael Kairis, Ismene Dontas, and Gregory Skalkeas Athens, Greece
Note from the Editor: Due to late author's alterations the abstract for this article has been omitted. INDEX WORDS: Tracheal stenosis; tracheoplasty.
X T E N S I V E T R A C H E A L stenosis is an obstructive lesion that can lead rapidly to life-threatening situations, especially in the small infant. Different techniques have been proposed to manage this serious condition such as endoscopic resection 1 with injection of steroids, 2 surgical resection and end-to-end anastomosis, 36 and dilatation plasties of the tracheal wall, both in clinical practice and in experimental animals. For these plasties, various tissues have been used such as pericardium, 7 esophagus, s cartilage, 9~~ etc, with results ranging from satisfactory to disappointing. We have used costal cartilage to treat tracheal stenosis in babies, with success. 11 Searching for a more easily handled tissue, in a pilot study with canines we used costal periosteum and sutured it to the tracheal gap with the osteogenic layer facing the lumen. The r~ults were disappointing. / T h e aim of the present study was to create an easily handled, semi-rigid, non-collapsible free periosteal graft, and use it in the reversed manner as a replacement graft to cover an oval-shaped artificial gap of the anterior trachea, as is the case after a longitudinal incision in extensive tracheal stenosi~z.(Furthermore, the long-term viability, functional 'laistopathologic changes, and biological behavior of the graft were studied.
E
intact periosteum. The periosteum was carefully removed from the rib, and a patch was created. Subsequently a mid low cervical incision was made, the local muscles were retracted and the trachea was revealed. An eliptical s e g m e n t ~ cm in length x 2 cm in width---of the anterior wall of the cervical trachea was excised, and a gap was created. The free periosteal graft was sutured to the margins of the defect using running 5-0 Prolene suture with the osteogenic layer facing toward the tracheal lumen in the first three dogs (group 1). In all others the flap was sutured in a reversed way. Care was taken to achieve an airtight suture line, and avoid stressing the graft to its full extent. The cervical muscles were re-approximated, and all skin incisions were closed with running 3-0 Prolene suture. At the end of the operation the endotracheal tube was removed. The operative time was approximately 90 minutes. The advantage of the above technique is that it can be performed within the same operative field in a short time without using an intratracheal stent. Broad spectrum antibiotics were started the day before surgery and continued four days post-operatively. All surviving animals received fluids for the day of operation and then were given a normal diet. Histology was done on all but one tracheal specimens of animals which died or were killed.
MATERIALS AND METHODS Twelve mongrel dogs weighing 7 to 10 kg were anesthetised with pentobarbital sodium, intubated, and ventilated artificially with a respirator. Under sterile conditions a right lateral transverse incision was performed at the level of the eighth rib. After separating the muscles a slice of the eighth rib 5 cm in length was cut and removed with its
From the Laboratory for Experimental Surgery and Surgical Research, Second Department of Prop. Surgery, School of Medicine, University of Athens; and the Departments of Pediatric Surgery and Pathology, Athens Children's Hospital, ",4 and P Kyriakou'" Goudi, Athens, Greece. Presented at the 35th Annual Congress of the British Association of Paediatric Surgeons, Athens, September 21-23, 1988. Address reprint requests to Christopher Moutsouris, MD, Patriarchou loakem 26a, Athens 10675, Greece. 9 1989 by Grune & Stratton, Inc. 0022-3468/89/2406-0014503.00/0 570
Fig 1. Extensive osteoplasia of the graft protruding in the tracheal lumen accompanied by moderate stenosis. Journal of Pediatric Surgery, Vol 24, No 6 (June), 1989: pp 570-572
REVERSED FREE PERIOSTEAL GRAFTING
RESULTS
None of the animals had an air leak at the anastomotic site or developed signs of airway obstruction at any stage following the operation. The first dog died on the seventh post-operative day. An autopsy revealed extensive sepsis involving the cervical area, and the graft as well. One more dog died unexpectedly on the 90th post-operative day. By mistake the dog was not sent for an autopsy so the cause of its death could not be determined. Of the surviving ten dogs, two with the osteogenic layer facing the lumen (group 1) were killed at 3 weeks, two of the reversed graft dogs (group 2) were killed at 3 weeks, two at 6 weeks, while the other four between the 60th and 75th post-operative day.
571
At autopsy in all animals of group 1, an osteoid protrusion of the graft towards the tracheal lumen, and a stenosis at the grafting site was noted (Fig 1). Light microscopy revealed an extensive osteoid metaplasia of the graft, while the inner surface was covered at a great extent by regenerated stratified ciliated epithelium (Fig 2). Autopsy in the group 2 dogs with the reversed periosteum revealed that the gap was completely bridged by the graft, which did not show any significant stenosis or osteoid hyperplasia protruding into the tracheal lumen (Fig 3). On light microscopy the gap was covered by fibroblastic connective tissue, while its inner surface was fully covered by regenerated stratified ciliated epithelium at the end of the sixth postoperative week (Fig 4). At the end of the tenth post-operative week the regenerated stratified ciliated epithelium was well differentiated, and in the outer collagenous connective tissue of the graft small foci of chondroplasia were noted. DISCUSSION
The advantage of semi-rigid, non-collapsible conduit for air, lined in its inner surface with respiratory epithelium, has been emphasised by many authors experienced in tracheal surgery) "4 Free periosteal grafts have already been used to cover tracheal defects either as a patch or encircling the trachea. ]214 In most of the published works the osteogenic layer of the periosteum was placed towards the tracheal lumen, and an intratracheal splint or the endotracheal tube was left in place post-operatively until proper healing was achieved.
Fig 2. Histology shows osteoplasia of the graft. The inner surface is lined by regenerating epithelium,
Fig 3. Inner surface of the reversed periosteal graft. No intraluminal protrusion or significant stenosis is noted.
572
MOUTSOURIS ET AL
entire procedure can be performed within the same operative field in a short period of time. Although we cannot offer an explanation for this distinct different behaviour of the reversed graft, it is obvious from this study that ossification already present at the end of the third post-operative week in the graft with the osteogenic layer facing the lumen, was not noted in the reversed graft even at the tenth post-operative week. However, the presence of small foci of chondrometaplasia in the graft of the animal sacrificed at 10 weeks post-operatively suggests t h a t the reverse graft posesses potentials of chondroosteometaplasia in the long term. This delayed potential might have beneficial effect on further strengthening of the tracheal wall. Although the results obtained by the above technique seem to be satisfactory, a long term study is in process to evaluate the delayed biological behaviour of the reversed periosteal graft. REFERENCES
Fig 4. The collagenous tissue of the reversed periosteal graft is lined by well-differentiated ciliated columnar epithelium w i t h goblet cell differentiation. Osteochondroplasia is not present.
In an earlier pilot study of canines, and in the first three animals of the present study, we also oriented the osteogenic layer of the graft facing the lumen of the trachea. O u r results obtained were not satisfactory. A n extensive osteoplasia of the graft protruding into the tracheal lumen was already present at 3 weeks, resulting in an obvious stenosis (Fig 1). However, respiratory epithelium had almost covered the biggest part of the graft at the same time (Fig 2). It is known that the periosteum is regarded as having two biologically distinct layers; an inner layer that possesses osteoblastic activity and an outer rather inactive fibrous layer. 15 In an effort to avoid the excessive osteoplasia, and stenosis observed in the first group of our animals we decided to apply the periosteal graft with the outer layer facing the lumen (reversed flap) to investigate the eventual effect on the mechanism of osteoplasia. With this modification we created a non-collapsible tracheal wall with perfect epithelisation of the mucosa, at the same time inhibiting osteoplasia and the resulting stenosis. With the use of costal periosteum, the
1. Benjamin B: Endoscopy in congenital tracheal anomalies. J Pediatr Surg 15:164-171, 1980 2. Othersen HB Jr: Steroid therapy for tracheal stenosis in children. Ann Thorac Surg 17:254-259, 1974 3. Besley R: Resection and reconstruction of the intrathoracic trachea. Br J Surg 38:200-205, 1950 4. Grillo HC: Tracheal reconstruction. Indication and techniques. Arch Otolaryngol 93:31-39, 1972 5. Mansfield PB: Tracheal resection in infancy. J Pediatr Surg 15:79-81, 1980 6. Mattingly WT, Belin RP, Todd EP: Surgical repair of congenital tracheal stenosis in an infant. J Thorac Cardiovasc Surg 81:738740, 1981 7. Idriss FS, Deleon SY, Ilbawi MN, et al: Tracheoplasty with pericardial patch for extensive tracheal stenosis in infants and children. J Thorac Cardiovasc Surg 88:527-536, 1984 8. Fonkalsrud EW, Sumida S: Tracheal replacement with autologous esophagus for tracheal structure. Arch Surg 102:139-42, 1971 9. Kimura K, Mukohara N, Tsugawa C, et al: Tracheoplasty for congenital stenosis of the entire trachea. J Pediatr Surg 17:869-871, 1982 10. Campbell ND, Lilly RJ: Surgery for total tracheal stenosis. J Pediatr Surg 21:934-935, 1986 11. Moutsouris Chr, Scondras K, Papageorgiou M, et al: Management of congenital extensive tracheal stenosis with free cartilage graft. Acta Chirurgica Hellenica (in press) 12. Kufaas T: Tracheal reconstruction with free periosteal grafts. An experimental study in rabbits. Scand J Thorac Cardiovasc Surg 31:1-63, 1981 (suppl) 13. Cohen CR, Filler MR, Konuma K, et al: The successful reconstruction of thoracic tracheal defects with free periosteal grafts. J Pediatr Surg 20:852-858, 1985 14. Haugen ES, Kufaas T, Svenningen S: Free periosteal grafts in tracheal reconstruction. An experimental study. Progr Pediatr Surg 21:47-49, 1987 15. McKibbin B: The biology of fracture healing in long bones. J Bone Joint Surg 60(B):150-162, 1978
Note from the Editor: Due to late author's alterations the abstract for this article has been omitted. INDEX WORDS: Tracheal stenosis; tracheoplasty.
X T E N S I V E T R A C H E A L stenosis is an obstructive lesion that can lead rapidly to life-threatening situations, especially in the small infant. Different techniques have been proposed to manage this serious condition such as endoscopic resection 1 with injection of steroids, 2 surgical resection and end-to-end anastomosis, 36 and dilatation plasties of the tracheal wall, both in clinical practice and in experimental animals. For these plasties, various tissues have been used such as pericardium, 7 esophagus, s cartilage, 9~~ etc, with results ranging from satisfactory to disappointing. We have used costal cartilage to treat tracheal stenosis in babies, with success. 11 Searching for a more easily handled tissue, in a pilot study with canines we used costal periosteum and sutured it to the tracheal gap with the osteogenic layer facing the lumen. The r~ults were disappointing. / T h e aim of the present study was to create an easily handled, semi-rigid, non-collapsible free periosteal graft, and use it in the reversed manner as a replacement graft to cover an oval-shaped artificial gap of the anterior trachea, as is the case after a longitudinal incision in extensive tracheal stenosi~z.(Furthermore, the long-term viability, functional 'laistopathologic changes, and biological behavior of the graft were studied.
E
intact periosteum. The periosteum was carefully removed from the rib, and a patch was created. Subsequently a mid low cervical incision was made, the local muscles were retracted and the trachea was revealed. An eliptical s e g m e n t ~ cm in length x 2 cm in width---of the anterior wall of the cervical trachea was excised, and a gap was created. The free periosteal graft was sutured to the margins of the defect using running 5-0 Prolene suture with the osteogenic layer facing toward the tracheal lumen in the first three dogs (group 1). In all others the flap was sutured in a reversed way. Care was taken to achieve an airtight suture line, and avoid stressing the graft to its full extent. The cervical muscles were re-approximated, and all skin incisions were closed with running 3-0 Prolene suture. At the end of the operation the endotracheal tube was removed. The operative time was approximately 90 minutes. The advantage of the above technique is that it can be performed within the same operative field in a short time without using an intratracheal stent. Broad spectrum antibiotics were started the day before surgery and continued four days post-operatively. All surviving animals received fluids for the day of operation and then were given a normal diet. Histology was done on all but one tracheal specimens of animals which died or were killed.
MATERIALS AND METHODS Twelve mongrel dogs weighing 7 to 10 kg were anesthetised with pentobarbital sodium, intubated, and ventilated artificially with a respirator. Under sterile conditions a right lateral transverse incision was performed at the level of the eighth rib. After separating the muscles a slice of the eighth rib 5 cm in length was cut and removed with its
From the Laboratory for Experimental Surgery and Surgical Research, Second Department of Prop. Surgery, School of Medicine, University of Athens; and the Departments of Pediatric Surgery and Pathology, Athens Children's Hospital, ",4 and P Kyriakou'" Goudi, Athens, Greece. Presented at the 35th Annual Congress of the British Association of Paediatric Surgeons, Athens, September 21-23, 1988. Address reprint requests to Christopher Moutsouris, MD, Patriarchou loakem 26a, Athens 10675, Greece. 9 1989 by Grune & Stratton, Inc. 0022-3468/89/2406-0014503.00/0 570
Fig 1. Extensive osteoplasia of the graft protruding in the tracheal lumen accompanied by moderate stenosis. Journal of Pediatric Surgery, Vol 24, No 6 (June), 1989: pp 570-572
REVERSED FREE PERIOSTEAL GRAFTING
RESULTS
None of the animals had an air leak at the anastomotic site or developed signs of airway obstruction at any stage following the operation. The first dog died on the seventh post-operative day. An autopsy revealed extensive sepsis involving the cervical area, and the graft as well. One more dog died unexpectedly on the 90th post-operative day. By mistake the dog was not sent for an autopsy so the cause of its death could not be determined. Of the surviving ten dogs, two with the osteogenic layer facing the lumen (group 1) were killed at 3 weeks, two of the reversed graft dogs (group 2) were killed at 3 weeks, two at 6 weeks, while the other four between the 60th and 75th post-operative day.
571
At autopsy in all animals of group 1, an osteoid protrusion of the graft towards the tracheal lumen, and a stenosis at the grafting site was noted (Fig 1). Light microscopy revealed an extensive osteoid metaplasia of the graft, while the inner surface was covered at a great extent by regenerated stratified ciliated epithelium (Fig 2). Autopsy in the group 2 dogs with the reversed periosteum revealed that the gap was completely bridged by the graft, which did not show any significant stenosis or osteoid hyperplasia protruding into the tracheal lumen (Fig 3). On light microscopy the gap was covered by fibroblastic connective tissue, while its inner surface was fully covered by regenerated stratified ciliated epithelium at the end of the sixth postoperative week (Fig 4). At the end of the tenth post-operative week the regenerated stratified ciliated epithelium was well differentiated, and in the outer collagenous connective tissue of the graft small foci of chondroplasia were noted. DISCUSSION
The advantage of semi-rigid, non-collapsible conduit for air, lined in its inner surface with respiratory epithelium, has been emphasised by many authors experienced in tracheal surgery) "4 Free periosteal grafts have already been used to cover tracheal defects either as a patch or encircling the trachea. ]214 In most of the published works the osteogenic layer of the periosteum was placed towards the tracheal lumen, and an intratracheal splint or the endotracheal tube was left in place post-operatively until proper healing was achieved.
Fig 2. Histology shows osteoplasia of the graft. The inner surface is lined by regenerating epithelium,
Fig 3. Inner surface of the reversed periosteal graft. No intraluminal protrusion or significant stenosis is noted.
572
MOUTSOURIS ET AL
entire procedure can be performed within the same operative field in a short period of time. Although we cannot offer an explanation for this distinct different behaviour of the reversed graft, it is obvious from this study that ossification already present at the end of the third post-operative week in the graft with the osteogenic layer facing the lumen, was not noted in the reversed graft even at the tenth post-operative week. However, the presence of small foci of chondrometaplasia in the graft of the animal sacrificed at 10 weeks post-operatively suggests t h a t the reverse graft posesses potentials of chondroosteometaplasia in the long term. This delayed potential might have beneficial effect on further strengthening of the tracheal wall. Although the results obtained by the above technique seem to be satisfactory, a long term study is in process to evaluate the delayed biological behaviour of the reversed periosteal graft. REFERENCES
Fig 4. The collagenous tissue of the reversed periosteal graft is lined by well-differentiated ciliated columnar epithelium w i t h goblet cell differentiation. Osteochondroplasia is not present.
In an earlier pilot study of canines, and in the first three animals of the present study, we also oriented the osteogenic layer of the graft facing the lumen of the trachea. O u r results obtained were not satisfactory. A n extensive osteoplasia of the graft protruding into the tracheal lumen was already present at 3 weeks, resulting in an obvious stenosis (Fig 1). However, respiratory epithelium had almost covered the biggest part of the graft at the same time (Fig 2). It is known that the periosteum is regarded as having two biologically distinct layers; an inner layer that possesses osteoblastic activity and an outer rather inactive fibrous layer. 15 In an effort to avoid the excessive osteoplasia, and stenosis observed in the first group of our animals we decided to apply the periosteal graft with the outer layer facing the lumen (reversed flap) to investigate the eventual effect on the mechanism of osteoplasia. With this modification we created a non-collapsible tracheal wall with perfect epithelisation of the mucosa, at the same time inhibiting osteoplasia and the resulting stenosis. With the use of costal periosteum, the
1. Benjamin B: Endoscopy in congenital tracheal anomalies. J Pediatr Surg 15:164-171, 1980 2. Othersen HB Jr: Steroid therapy for tracheal stenosis in children. Ann Thorac Surg 17:254-259, 1974 3. Besley R: Resection and reconstruction of the intrathoracic trachea. Br J Surg 38:200-205, 1950 4. Grillo HC: Tracheal reconstruction. Indication and techniques. Arch Otolaryngol 93:31-39, 1972 5. Mansfield PB: Tracheal resection in infancy. J Pediatr Surg 15:79-81, 1980 6. Mattingly WT, Belin RP, Todd EP: Surgical repair of congenital tracheal stenosis in an infant. J Thorac Cardiovasc Surg 81:738740, 1981 7. Idriss FS, Deleon SY, Ilbawi MN, et al: Tracheoplasty with pericardial patch for extensive tracheal stenosis in infants and children. J Thorac Cardiovasc Surg 88:527-536, 1984 8. Fonkalsrud EW, Sumida S: Tracheal replacement with autologous esophagus for tracheal structure. Arch Surg 102:139-42, 1971 9. Kimura K, Mukohara N, Tsugawa C, et al: Tracheoplasty for congenital stenosis of the entire trachea. J Pediatr Surg 17:869-871, 1982 10. Campbell ND, Lilly RJ: Surgery for total tracheal stenosis. J Pediatr Surg 21:934-935, 1986 11. Moutsouris Chr, Scondras K, Papageorgiou M, et al: Management of congenital extensive tracheal stenosis with free cartilage graft. Acta Chirurgica Hellenica (in press) 12. Kufaas T: Tracheal reconstruction with free periosteal grafts. An experimental study in rabbits. Scand J Thorac Cardiovasc Surg 31:1-63, 1981 (suppl) 13. Cohen CR, Filler MR, Konuma K, et al: The successful reconstruction of thoracic tracheal defects with free periosteal grafts. J Pediatr Surg 20:852-858, 1985 14. Haugen ES, Kufaas T, Svenningen S: Free periosteal grafts in tracheal reconstruction. An experimental study. Progr Pediatr Surg 21:47-49, 1987 15. McKibbin B: The biology of fracture healing in long bones. J Bone Joint Surg 60(B):150-162, 1978