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Figure 1.
The thyroid alar cartilage graft procedure showing harvesting of the superior aspect of the thyroid ala. Note that the inner perichondrium is preserved.

The thyroid alar cartilage graft procedure showing harvesting of the superior aspect of the thyroid ala. Note that the inner perichondrium is preserved.

Figure 2.
The thyroid alar cartilage graft procedure showing graft preparation and application. The graft outer perichondrial layer is placed facing the subglottic lumen.

The thyroid alar cartilage graft procedure showing graft preparation and application. The graft outer perichondrial layer is placed facing the subglottic lumen.

Figure 3.
A transverse section of thyroid alar cartilage graft 6 weeks after graft placement showing the graft anteriorly (hematoxylin-eosin, original magnification ×10).

A transverse section of thyroid alar cartilage graft 6 weeks after graft placement showing the graft anteriorly (hematoxylin-eosin, original magnification ×10).

Figure 4.
A transverse section of costal cartilage graft 6 weeks after graft placement showing the graft anteriorly (hematoxylin-eosin, original magnification ×10).

A transverse section of costal cartilage graft 6 weeks after graft placement showing the graft anteriorly (hematoxylin-eosin, original magnification ×10).

Figure 5.
A transverse section of auricular cartilage graft 6 weeks after graft placement showing the graft anteriorly (hematoxylin-eosin, original magnification ×10).

A transverse section of auricular cartilage graft 6 weeks after graft placement showing the graft anteriorly (hematoxylin-eosin, original magnification ×10).

Table 1. 
Data for Group Having Thyroid Alar Cartilage Graft for Laryngotracheal Reconstruction*
Data for Group Having Thyroid Alar Cartilage Graft for Laryngotracheal Reconstruction*
Table 2. 
Data for the Group Having Costal Cartilage Graft for Laryngotracheal Reconstruction*
Data for the Group Having Costal Cartilage Graft for Laryngotracheal Reconstruction*
Table 3. 
Data for the Group Having Auricular Cartilage Graft for Laryngotracheal Reconstruction*
Data for the Group Having Auricular Cartilage Graft for Laryngotracheal Reconstruction*
1.
Rethi  A An operation for cicatricial stenosis of the larynx. J Laryngol. 1956;70283- 293Article
2.
Lapidot  ASodagar  RRatanaprashtporn  SSilverman  R Experimental repair of subglottic stenosis in piglets. Arch Otolaryngol. 1968;88529- 535Article
3.
Fearon  BCotton  R Surgical correction of subglottic stenosis of the larynx. Ann Otol Rhinol Laryngol. 1972;81508- 513
4.
Fearon  BCotton  R Subglottic stenosis in infants and children: the clinical problem and experimental surgical correction. Can J Otolaryngol. 1972;1281- 289
5.
Fearon  BCotton  R Surgical correction of subglottic stenosis of the larynx in infants and children: progress report. Ann Otol Rhinol Laryngol. 1974;83428- 431
6.
Toohill  RJMartinelli  DLJanowak  MC Repair of laryngeal stenosis with nasal septal grafts. Ann Otol Rhinol Laryngol. 1976;85 (pt 1) 600- 608
7.
Finnegan  DAWong  MLKashima  HK Hyoid autograft repair of chronic subglottic stenosis. Ann Otol Rhinol Laryngol. 1975;84 (pt 1) 643- 649
8.
Strome  MNorris  CMJoseph  MPBrodsky  GEavey  RD An assessment of grafts in the posterior cricoid lamina. Laryngoscope. 1982;92 (pt 1) 1120- 1125Article
9.
Zehm  S The use of composite grafts for reconstruction of the trachea and subglottic airway. Trans Am Acad Ophthalmol Otolaryngol. 1977;84ORL934- ORL940
10.
Zalzal  GHCotton  RTMcAdams  AJ The survival of costal cartilage graft in laryngotracheal reconstruction. Otolaryngol Head Neck Surg. 1986;94204- 211
11.
Cotton  RT The problem of pediatric laryngotracheal stenosis: a clinical and experimental study on the efficacy of autogenous cartilaginous grafts placed between the vertically divided halves of the posterior lamina of the cricoid cartilage. Laryngoscope. 1991;101 (pt 2 suppl 56) 1- 34Article
12.
Wiatrak  BJAlbert  DMHolmes  DKCotton  RT Cartilage graft epithelialization: a preliminary study using a goat model. Arch Otolaryngol Head Neck Surg. 1993;119777- 781Article
13.
Bean  JKVerwoerd-Verhoef  HLVerwoerd  CD Reconstruction of the anterior laryngeal wall with a composite graft of demineralized bovine bone matrix and autogenous perichondrium: an experimental study in adult rabbits. ORL J Otorhinolaryngol Relat Spec. 1994;56224- 229Article
14.
Lusk  RPKang  DRMuntz  HR Auricular cartilage grafts in laryngotracheal reconstruction. Ann Otol Rhinol Laryngol. 1998;102 (pt 1) 247- 254
15.
Fry  TLFischer  NDPillsbury  HC Tracheal reconstruction with pedicled thyroid cartilage. Laryngoscope. 1985;9560- 62Article
16.
Rice  DHColman  M Repair of subglottic stenosis with a free perichondrial graft. Arch Otolaryngol. 1982;10825- 27Article
17.
Park  AHForte  V The effects of harvesting autogenous laryngeal cartilage for laryngotracheal reconstruction on laryngeal growth and support. Laryngoscope. In press.
Original Article
January 2000

Comparison of Thyroid, Auricular, and Costal Cartilage Donor Sites for Laryngotracheal Reconstruction in an Animal Model

Author Affiliations

From the Departments of Otorhinolaryngology and Communicative Sciences (Dr de Jong) and Pathology (Dr Schwartz), Baylor College of Medicine, Houston, Tex; the Department of Otolaryngology–Head and Neck Surgery, Loyola University Medical Center, Maywood, Ill (Dr Park); and the Department of Pediatric Otolaryngology, Hospital for Sick Children, Toronto, Ontario (Drs Raveh and Forte).

Arch Otolaryngol Head Neck Surg. 2000;126(1):49-53. doi:10.1001/archotol.126.1.49
Abstract

Objective  To evaluate and compare the use of autogenous thyroid cartilage with that of auricular and costal cartilage in laryngotracheoplasty (LTP).

Design  A blinded comparison of LTP techniques using anterior thyroid, auricular, or costal cartilage as graft material in a rabbit model. Histological and anatomical analyses were performed on the laryngeal specimens 1, 4, and 6 weeks after surgery. The following factors were analyzed in each specimen: graft viability, cartilage proliferation, perichondrial viability, degree of necrosis, inflammatory response, and degree of epithelialization.

Subjects  Fifty-seven New Zealand adult male rabbits, aged 6 months, were divided into 3 study groups (19 animals in each group) initially and equally into the 3 time periods.

Results  No episodes of respiratory compromise occurred in any of the animals in the 3 study groups. Gross inspection of the laryngotracheal complex in the thyroid cartilage group revealed no evidence of laryngeal structural compromise. There was no statistical difference between the 3 types of cartilage used for reconstruction for the variables of graft or perichondrial viability, degree of necrosis, or inflammatory response at 1, 4, or 6 weeks. Cartilage proliferation in the thyroid cartilage group was decreased compared with that in the other 2 groups at 1 week. The amount of proliferation increased in this group and was equal to the amount present in the other 2 groups 4 and 6 weeks after surgery. Complete epithelialization of the graft material was present in all 3 groups at 4 and 6 weeks after reconstruction.

Conclusions  The use of autogenous thyroid cartilage for LTP compares favorably with that of other methods of reconstruction that use either auricular or costal cartilage in the rabbit model. This technique is a viable alternative for single-stage LTP and has the added advantage of using a single incision.

DURING THE past 30 years, the treatment of severe subglottic stenosis has evolved into the now widely accepted concept of surgical expansion of the stenotic laryngeal lumen. Early methods, pioneered by Rethi1 in 1956, focused on splitting the cartilaginous skeleton. In 1969, Lapidot et al2 reported on a method of repairing subglottic stenosis in piglets that used an interposition technique. Fearon and Cotton35 extended the experimental work of Lapidot et al and popularized the method of anteriorly splitting the thyrocricoid complex and placing autogenous graft material in children. Their technique—laryngotracheoplasty (LTP)—has become an accepted method for treating severe subglottic stenosis.

The best augmentation material for LTP remains controversial. Many autogenous grafts have been described.610 Ideally, the graft material should be malleable to permit carving and shaping, but firm enough to stent the anterior cricoid and tracheal cartilage open. The autogenous material should be similar to tissue in the area. It should hold sutures well and be easy to harvest. The graft harvest should be associated with minimal donor site morbidity and preferably be obtained through the same operative incision used for graft placement.

Costal and auricular cartilages are the most common augmentation materials used in the LTP procedures.11,12 Donor site discomfort and morbidity are well-documented problems when either rib or ear cartilage is used in LTP procedures.13,14 To our knowledge, no one has described the use of an anterior thyroid lamina cartilage graft in single-stage laryngotracheal reconstruction. This type of graft offers several advantages, particularly the use of a single operative incision. It is obtained during the approach to the laryngotracheal complex for an LTP procedure. The thyroid alar cartilage (TAC) is firm but is easily shaped and carved.

The purpose of the present study is to evaluate the use of TAC as a graft material for anterior LTP procedures. In an animal model, the use of a TAC graft for cricoid expansion was evaluated and compared with that of 2 other well-accepted autogenous graft materials, auricular and costal cartilage.

ANIMALS AND METHODS

Fifty-seven white New Zealand adult male rabbits, aged 6 months, were used in this investigation. Their preoperative mean weight was 4.0 kg (range, 3.3-4.4 kg). The animals were divided into 3 groups of 19 animals each. All animals underwent anterior LTP procedures with the use of auricular, costal, or TAC grafts.

SURGICAL TECHNIQUE

On the day of surgery, each rabbit received premedication consisting of subcutaneously administered atropine sulfate (3 mg), followed by apromazine (0.18 mg/kg) and xylazine hydrochloride (0.18 mg/kg) administered intramuscularly. The animals were intubated, and anesthesia was maintained with the use of 2% halothane. Sterile conditions were maintained throughout all operative procedures. Auricular and costal cartilages were harvested using the methods of Cotton11 and Wiatrak et al.12 A 20-mm section of cartilaginous rib was harvested. A section of auricular cartilage 10 × 10 mm was removed. The ventral perichondrial layer was included and preserved on each graft.

The TAC graft was obtained through the LTP incision. A vertical midline incision was made over the larynx and upper trachea, and the airway was exposed. The TAC graft was harvested as follows: the anterior aspect of the thyroid cartilage was exposed and examined. A 5×8-mm section of cartilage was removed from the superior aspect of the left thyroid lamina (Figure 1). Care was taken to leave the medial, or inner, layer of the perichondrium intact. The ventral, or lateral, surface of the perichondrium was harvested with the graft. After the grafts were harvested from 1 of the 3 locations, the material was then sculpted into a 5×8-mm piece with tapered ends (Figure 2).

The laryngotracheal complex was exposed for the costal and auricular graft models using the incision described for the TAC graft. Then a vertical midline incision was made in the cricoid cartilage and first tracheal ring, and the preshapened graft was interposed between the cut edges of the cricoid cartilage and tracheal ring. The graft was positioned with the perichondrial layer facing the airway lumen (Figure 2). The graft was fixed in position with 5-0 polydioxanone sutures. The neck incision was closed in layers using 4-0 Vicryl sutures. Each animal was extubated at the conclusion of the operative procedure.

The animals in each group were then evenly distributed within 1 of 3 subsets based on the time to laryngeal harvest: 1, 4, and 6 weeks. At the various time points from the date of the surgery, the animals were killed. The larynges were harvested and transversely sectioned through the region of the cartilage graft. The sections were stained with hematoxylin-eosin, and histological analysis was performed.

All procedures were conducted humanely and approved by the Institutional Animal Care and Use committees of the University of Toronto School of Medicine and the Hospital for Sick Children, Toronto, Ontario.

HISTOLOGICAL ANALYSIS

Six histological variables were observed and graded in each specimen. The pathologist (M.R.S.) was blinded to the graft material and to the duration of graft placement in each animal. The following variables were analyzed: graft viability (nonviable = 0 and viable = 1), cartilage proliferation (none = 0 and active proliferation = 1), perichondrial layer (not intact = 0 and intact = 1), degree of necrosis (minimal = 1, moderate = 2, and severe = 3), inflammatory response (minimal = 1, moderate = 2, and severe = 3), and epithelialization of the intraluminal graft surface (<25% = 0, 26%-50% = 1, 51%-75% = 2, and >75% = 3).

We used the Kruskal-Wallis test for the statistical analysis of all histological variables with the aid of a statistical software program (Minitab version 12.1; Minitab, Inc, State College, Pa), with P<.05 considered significant.

RESULTS
OBSERVATIONS

No episodes of respiratory compromise occurred in any of the animals studied. Seven animals died in the early postoperative period. Three animals in the group having costal cartilage graft died (2 in the 1-week and 1 in the 4-week subsets), and 3 animals in the group having auricular cartilage graft died (2 in the 1-week and 1 in the 4-week subsets). An additional rabbit from the group having TAC graft (1-week subset) also died. All animals that died prematurely failed to maintain oral feeding, with no evidence of respiratory distress in any of these animals. Autopsies were not performed.

Gross inspection of the laryngotracheal complex at the time of harvest revealed a widely patent airway in all animals studied in all 3 graft material groups at all intervals (Figure 3, Figure 4, and Figure 5).

HISTOLOGICAL ANALYSIS

The histological data for the 3 study groups are summarized in Table 1, Table 2, and Table 3. Changes observed due to surgical trauma or suture granulomas were excluded from analysis. At 1, 4, and 6 weeks, no significant differences occurred between the TAC graft, costal cartilage graft, or auricular cartilage graft for the graft viability, the presence of the perichondrial layer, the degree of necrosis, or the inflammatory response. Decreased cartilage proliferation (eg, new cartilage formation) was noted in 1 week for the group having the TAC graft compared with the groups having auricular and costal cartilage grafts (P = .03 and P = .01, respectively). The level of new cartilage formation increased from 1 to 4 weeks in the TAC graft group. The difference between the 3 graft material groups was not significant by 4 weeks. A trend toward earlier graft epithelialization was observed in the group having the costal cartilage graft compared with the other 2 groups. Complete graft epithelialization was present in most of the animals in all 3 groups by 6 weeks after graft placement. No viable graft cartilage was found in 3 of the animals in the group with the costal cartilage graft (Table 2, specimens F, N, and O) and 2 of the specimens from the group with the TAC graft (Table 1, specimens A and O). Although new cartilage formation was seen in 3 of the 4 animals, the new cartilage was found in association with the cut edges of the native laryngotracheal cartilage.

COMMENT

No single, consistently successful, method of repair for subglottic stenosis has been devised. Several methods that use TAC have previously been described. Pedicled TAC was proposed as a graft material for cricoid expansion, first by Fearon and Cotton3 and then later by Fry et al.15 Whereas the idea of a muscle pedicled graft with its own blood supply and mucoperichondrium is attractive, in practice, it is not a good option in small children due to limitations in size. Free TAC grafts in the posterior cricoid lamina were evaluated in dogs by Strome et al8 and found not to be beneficial. Rice and Colman16 described the use of a free thyroid alar perichondrial graft in dogs with and without stents. They found that in 9 of 10 animals studied, the amount of cartilage formed from the free perichondrial graft was adequate to bridge the airway. The shape of the subglottic lumen, however, was unpredictable.17

This animal study was undertaken to evaluate the use of a TAC graft in laryngotracheal reconstruction compared with 2 other well-accepted graft materials (auricular and costal cartilages). The TAC graft compared favorably with both the auricular and costal cartilage graft models.

One problem with the present study is the limited sample size in each group. The small number makes statistical evaluation difficult and could also explain why no significant difference was found between groups.

Using an autogenous TAC graft offers many theoretical advantages compared with other techniques. Superior thyroid cartilage lamina is nearly identical in thickness to the cricoid cartilage. The similar thickness decreases the possibility of prolapse of the graft material into the tracheal lumen. The perichondrium is harvested with the lateral surface of the thyroid cartilage and can be positioned facing intraluminally when the graft is sutured in place. This provides a surface for epithelialization that limits the potential for the formation of granulation tissue. Most important, the graft is harvested through the same neck incision used to expose the cricoid cartilage, eliminating the need for a second operative site. Possible disadvantages of the TAC graft include limitations of the size of the graft, destabilization of the laryngeal skeleton, and alteration in the growth of the thyroid lamina. No evidence of donor site morbidity was observed up to 6 weeks after cartilage harvest. A recent animal study17 indicates that removing the superior portion of TAC does not affect laryngeal growth. Viable perichondrium, however, is well known10,16,17 to induce neocartilage formation. The inner perichondrium at the superior aspect of the TAC donor site is carefully preserved to promote the generation of new cartilage. Although the present study is applicable only to an animal model, future investigations will focus on the application of this technique in the pediatric airway.

In conclusion, the use of autogenous TAC graft represents a viable option and alternative for single-stage cricoid expansion procedures and has the added advantage of using a single incision.

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Article Information

Accepted for publication May 14, 1999.

Presented in part at the annual meeting of the American Society of Pediatric Otolaryngology, Palm Beach, Fla, May 14, 1998.

Reprints: Andrew L. de Jong, MD, Department of Otorhinolaryngology and Communicative Sciences, Baylor College of Medicine, Texas Children's Hospital, The Feigin Center, 1102 Bates St, Suite 340, Houston, TX 77030.

References
1.
Rethi  A An operation for cicatricial stenosis of the larynx. J Laryngol. 1956;70283- 293Article
2.
Lapidot  ASodagar  RRatanaprashtporn  SSilverman  R Experimental repair of subglottic stenosis in piglets. Arch Otolaryngol. 1968;88529- 535Article
3.
Fearon  BCotton  R Surgical correction of subglottic stenosis of the larynx. Ann Otol Rhinol Laryngol. 1972;81508- 513
4.
Fearon  BCotton  R Subglottic stenosis in infants and children: the clinical problem and experimental surgical correction. Can J Otolaryngol. 1972;1281- 289
5.
Fearon  BCotton  R Surgical correction of subglottic stenosis of the larynx in infants and children: progress report. Ann Otol Rhinol Laryngol. 1974;83428- 431
6.
Toohill  RJMartinelli  DLJanowak  MC Repair of laryngeal stenosis with nasal septal grafts. Ann Otol Rhinol Laryngol. 1976;85 (pt 1) 600- 608
7.
Finnegan  DAWong  MLKashima  HK Hyoid autograft repair of chronic subglottic stenosis. Ann Otol Rhinol Laryngol. 1975;84 (pt 1) 643- 649
8.
Strome  MNorris  CMJoseph  MPBrodsky  GEavey  RD An assessment of grafts in the posterior cricoid lamina. Laryngoscope. 1982;92 (pt 1) 1120- 1125Article
9.
Zehm  S The use of composite grafts for reconstruction of the trachea and subglottic airway. Trans Am Acad Ophthalmol Otolaryngol. 1977;84ORL934- ORL940
10.
Zalzal  GHCotton  RTMcAdams  AJ The survival of costal cartilage graft in laryngotracheal reconstruction. Otolaryngol Head Neck Surg. 1986;94204- 211
11.
Cotton  RT The problem of pediatric laryngotracheal stenosis: a clinical and experimental study on the efficacy of autogenous cartilaginous grafts placed between the vertically divided halves of the posterior lamina of the cricoid cartilage. Laryngoscope. 1991;101 (pt 2 suppl 56) 1- 34Article
12.
Wiatrak  BJAlbert  DMHolmes  DKCotton  RT Cartilage graft epithelialization: a preliminary study using a goat model. Arch Otolaryngol Head Neck Surg. 1993;119777- 781Article
13.
Bean  JKVerwoerd-Verhoef  HLVerwoerd  CD Reconstruction of the anterior laryngeal wall with a composite graft of demineralized bovine bone matrix and autogenous perichondrium: an experimental study in adult rabbits. ORL J Otorhinolaryngol Relat Spec. 1994;56224- 229Article
14.
Lusk  RPKang  DRMuntz  HR Auricular cartilage grafts in laryngotracheal reconstruction. Ann Otol Rhinol Laryngol. 1998;102 (pt 1) 247- 254
15.
Fry  TLFischer  NDPillsbury  HC Tracheal reconstruction with pedicled thyroid cartilage. Laryngoscope. 1985;9560- 62Article
16.
Rice  DHColman  M Repair of subglottic stenosis with a free perichondrial graft. Arch Otolaryngol. 1982;10825- 27Article
17.
Park  AHForte  V The effects of harvesting autogenous laryngeal cartilage for laryngotracheal reconstruction on laryngeal growth and support. Laryngoscope. In press.
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