International Elsevier
Journal of Pediatric Otorhinola~ngology,
17 (1989) 213-224
213
PEDOT 00582
Independent effects of denervating the cricothyroid muscle and stenting on the anterior cricoid split: canine model Craig W. Senders ’ and Pam Eisele 2 ’ Department of Otolaryngology - Head and Neck Surgery, University of California, Dauis Medical Center, Sacramento,
CA 95817 (U.S.A.) and 2 Primate Center, University of California, Dauis, CA 95616 (U.S.A.) (Received 23 August 1988) (Accepted 2 February 1989)
Key words: Cricoid cartilage; Endotracheal tube stent; Subglottic size; Subglottic stenosis
Abstract
The anterior cricoid split (ACS) has gained in popularity since its introduction in 1980, for the treatment of the difficult to extubate child. The procedure allows a successful extubation and avoids a tracheotomy about 75% of the time. How the ACS allows extubation remains poorly understood. Animal research has shown that in the canine model the ACS results in a gap in the cricoid cartilage with a subjective increase in the subglottic space (Senders and Eisele, 1987). This gap in the cricoid cartilage develops whether or not an endotracheal tube stent is used. This experiment was designed to quantitatively evaluate the effect of the ACS on the subglottic space with or without the use of the stent, and to evaluate the effect of the cricothyroid muscle on the ACS procedure. The results show that the ACS does result in an increase in the subcricoid space, and that the use of an endotracheal tube stent does result in a larger increase. The cricothyroid muscle has a strong immediate effect on the gap in the cricoid cartilage, which is eliminated by sectioning the external laryngeal nerve. The long-term effects of sectioning the external laryngeal nerve on the gap in the cricoid cartilage were not conclusive.
Correspondence: C.W. Senders, Department of Otolaryngology-Head and Neck Surgery, University of California, Davis Medical Center, 2500 Stockton Blvd. Sacramento, CA 95817, U.S.A.
0165-5876/89/%03.50
0 1989 Elsevier Science Publishers B.V.
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Introduction In 1980, Cotton and Seid introduced a new surgical procedure, the anterior cricoid split (ACS), for the treatment of the difficult to extubate infant or child [2]. The original procedure was about 75% successful in allowing extubation and avoiding a tracheotomy. Since the introduction of the ACS, several other authors have shown similar success rates [3-57-91. Animal research on the topic has been limited. Senders and Bisele, using a canine model showed that the ACS did result in a gap in the cricoid cartilage 5 weeks after removal of the stent [8]. In addition, they showed that the ACS with a stent produced a larger gap in the cricoid cartilage than the ACS operation alone. Subjectively they felt that there was an increase in the subglottic space after the procedure, but this was not analyzed quantitatively. Babyak et al. performed a descriptive study using the canine model [l]. They demonstrated the ACS resulted in a gap in the cricoid cartilage as early as 7 days and that this gap persisted up to 6 months. Their work confirmed Senders and Bisele’s observations that the gap occurred whether or not the stent was used. Seven days after the ACS (day of stent removal) the gap in the cricoid cartilage resulted in a 26% increase in the subglottic space (4 animals studied). Long-term quantitative analysis of the subglottic size was not performed. On the basis of our previous work and the work of Babyak et al., we postulate that the gap in the cricoid cartilage is not a direct result of the stent but rather is a result of contraction of the intrinsic laryngeal muscles, specifically the cricothyroid muscle and the lateral cricoarytenoid muscle. This is supported by the findings that the ACS alone without a stent produces a gap in the cricoid cartilage. Also when the stent is used the ultimate gap in the cricoid cartilage is significantly larger than the gap initially induced by the stent at the time of surgery. In this setting the stent may be acting more as an irritant causing coughing which would stimulate both the cricothyroid muscle and the lateral cricoarytenoid muscle. The following experiment was designed to look at 3 questions regarding the ACS: 1. Does the ACS result in an increase in the subglottic space? 2. Does the ACS with stenting result in a greater increase in subglottic space than the ACS alone? 3. Does denervating the cricothyroid muscle by sectioning the external laryngeal nerve (ELN) have an effect on the ACS?
Materials and methods Thirty-seven 6-7-week-old, weaned, mongrel puppies from 5 litters were utilized for this experiment. Because of the genetic variability inherent in using mongrel animals, the size varied from 0.8 kg to 3.8 kg with a mean of 1.9 kg and a standard deviation of 0.8 kg. The animals were housed indoors where the temperature and lights were controlled and were fed a moistened commercial puppy diet.
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Animals were randomly assigned to 4 groups. Seven animals were assigned to Group 1 which served as controls; 10 animals were assigned to Group 2 which received the ACS operation with sectioning of the external laryngeal nerve; 11 animals were assigned to Group 3 which underwent the ACS procedure alone; and 9 animals were assigned to Group 4 which underwent the ACS procedure with insertion of a stent for 7 days. The day of surgery was considered day number 0 and all animals received Septra orally for the first 7 days of the study. All animals in Groups 2, 3, and 4 underwent a surgical procedure. The premedications included atropine (0.04 mg/kg s.c.) and Innovar-Vet (0.1 ml/kg i.m.). General anesthesia was achieved by titrating with pentobarbital and supplementing when necessary (6 mg/kg initial dose). The neck area was shaved and the animals were placed on a heating blanket in the supine position with the neck extended. After a sterile prep and draping, an incision was made through the skin and subcutaneous tissue and the strap muscles were divided in the ventral midline of the neck exposing the thyroid cartilage, cricoid cartilage, and the cranial 5-7 tracheal rings. Following this, a longitudinal incision was made through the cricoid cartilage and the mucosa into the subglottic lumen. The incision was extended through the first and second tracheal rings caudally and to the thyroid cartilage cranially. The resting gap in the cricoid cartilage was measured using calipers. The dissection was then carried laterally to expose the external laryngeal nerve (ENL) bilaterally. In Group 2 (ACS with ELN section) the identity of ELN was confirmed with a nerve stimulator and sectioned bilaterally. An agonal contraction of the cricothyroid muscle confirmed proper sectioning in all animals. The gap in the cricoid cartilage was then remeasured. The incision was then closed loosely with nylon sutures which reapproximated both the strap muscles and the skin. In Group 3 (ACS alone) the skin incision was closed loosely with nylon sutures which reapproximated the strap muscles and the skin. In Group 4 (ACS with stent) a modified polyvinylchloride endotracheal tube (Anmerican Hospital Supply) was inserted orally by a surgical assistant. The endotracheal tubes were 3i cm in length and both edges were smoothed and beveled. The tube was carefully positioned such that it extended through the true vocal cords but not above the false vocal cords (Fig. 1). Thus, during swallowing the false vocal cords and epiglottis helped present aspiration (Fig. 2). The tube size was chosen such that the gap in the cricoid cartilage measured between 2.0 and 3.5 mm after the endotracheal tube was inserted. A nylon suture placed over buttons was then passed transcutaneously through the strap muscles, the trachea and the endotracheal tube at the approximate level of the sixth tracheal ring to secure the tube into position. The wound was then loosely closed with nylon sutures. No drains or bandages were used. The animals were offered water the evening following surgery, and thereafter a moistened puppy diet as tolerated. The animals were carefully monitored for dehydration, aspiration, and signs of pneumonia postoperatively. If indicated, animals were hand-fed. Seven days after the initial procedure the endotracheal tube was removed from Group 4 (ACS with stent) and the skin sutures were removed from Groups 2, 3, and 4 using a short-acting intravenous anesthetic of diazepam and ketamine.
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Fig. 1. Stent is sutured in place with a transcutaueous and transtracheal suture. The cephalad portion of the stent lies between the true vocal cords (TVC) and false vocal cords (FVC).
Five weeks after the initial procedures, all animals were euthanized with intravenous pentobarbital. The larynx and 6 tracheal rings were removed (Fig. 3). The diameters of the trachea, the fourth tracheal ring, and the gap in the cricoid cartilage were measured with calipers. The larynx was then fixed in Kamovsky solution. After fixation, horizontal sections were cut through the subgIottic region. These sections were then decalcified in EDTA for 4 weeks prior to paraffin embedding and H&E staining [6]. After fixation, the first tracheal ring had retracted to lie inside the cricoid cartilage. Therefore, subglottic lumenal area measurements were felt to be an inaccurate estimate of the premorbid subglottic size. Area measurements were taken to be the entire area lying inside the cricoid cartilage. Where a gap was present in the cricoid cartilage (Groups 2, 3, and 4) a horizontal line connecting the gap was utilized to complete the ring. All area
NORMAL Fig. 2. During respiration
SWALLOWING
the airway remains open. With swallowing minimizes aspiration.
the subglottis covers the stent and
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measurements were made from black and white photographs of the histologic sections using a digitizing tablet (Kurta Corporation, Model 204689) and analyzed on an IBM-compatible computer using Via (Ted Pella Inc.).
Results The raw data are presented in Table I. The use of mongrel animals increased the variability within each experimental group. A two-way analysis of variance showed a significant effect of the animals’ weights, litter from which they came, and tracheal size on the experimental outcome (P -c 0.05). In analyzing the data, ratios were utilized in most comparisons where the experimental results were divided by the animal’s preoperative weight or tracheal size to minimize the variance. The immediate effect of sectioning the ELN was determined in Group 2. Without a stent in place, intraoperative cricoid gap measurements were taken prior to and
TABLE I Data
of the 4 groups used in our experiment
I (Control)
II (ACS)
Trach size (mm)
Wl. (kg)
11.5 15.0 12.5 14.0 14.5 14.0 16.5
0.8 1.8 1.2 1.6 1.7 1.7 2.8
Cricoid gap (mm)
Subcricoid area (mm2)
Trach size (mm)
Wt. (kg)
Cricoid gap (mm)
Subcricoid area (mm’)
98.3 139.9 99.4 117.4 96.2 98.4 182.6
14.5 14.0 15.0 15.0 15.0 13.0 11.0 13.5 14.0 14.5 16.0
1.8 1.6 1.4 1.5 1.9 1.2 0.9 1.9 1.8 3.4 3.7
1.5 1.0 0.3 2.0 4.0 4.0 5.5 7.0 4.5 16.0 11.5
152.2 138.0 135.7 160.1 145.1 123.5 92.6 125.6 126.8 157.9 168.2
Cricoid gap (mm)
Subcricoid area (mm2)
III (AC.!? with ELN cut)
IV (ACS
with stent)
Trach size (mm)
wt. (kg)
Cricoid gap (mm)
Subcricoid area (mm*)
Trach size (mm)
wt. (kg)
14.0 14.0 14.0 15.0 12.0 12.5 13.5 14.5 14.5 14.0
1.5 1.7 1.6 1.8 0.9 1.5 2.2 2.2 3.3 3.3
0.7 1.0 1.2 1.5 2.5 2.0 3.0 1.0 4.0 6.5
124.5 112.0 137.3 145.8 89.4 119.9 140.7 127.0 133.6 151.5
11.5 13.0 14.0 15.0 13.0 12.0 16.0 16.0
1.1 1.8 1.6 1.5 1.2 1.3 2.1 3.8
8.5 6.0 6.5 9.0 9.5 5.5 10.0
123.1 133.7 158.8 163.5 136.1 142.6 135.2 120.1
Fig. 3. Representative examples of each experimental graup 5 weeks after procedure. A: control; B: ACS with ELN section; C: ACS alone; D: ACS with stent.
Fig. 4. Prior to sectioning the external laryngeal nerve there was a gap in the cricaid cartilage (arrow).
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0
Gap/Wt
T
6
0 g a
5 4 3 2 1 0
Control
ACS-ELN
ACS
ACS
Stent
Fig. 5. Ratio of cricoid gap to animal weight. P < 0.01 when comparing group 4 (ACS with stent) with groups 2 (ACS with ELN section) or 3 (ACS alone).
after sectioning of the external laryngeal nerve (ELN) (Fig. 4). Prior to sectioning the mean cricoid gap was 1.3 mm with a standard deviation of 1.1 mm. The postsectioning mean gap was 0.5 mm with a standard deviation of 0.2 mm. A “t “-test for matched pairs (t = 3.2, df = 10, r = 0.74, r* = 0.55) shows this to be highly significant (P < 0.01). The long-term (5 weeks postsurgery) effect of the various treatments on the gap in the cricoid cartilage was determined by forming a ratio of the cricoid gap divided by the anirnaI’s preoperative weight (Fig. 5). In Group 1 (controls) the ratio was 0. In Group 2 (ACS with ELN section) the ratio was 1.2 with a standard deviation of 0.7. Group 3 (ACS alone) showed a ratio of 2.6 with a standard deviation of 1.8. Group 4 (ACS with stent) shows a ratio of 5.1 with a standard deviation of 2.2 (Fig. 6). A one way analysis of variance shows that F3,32 = 16.9. Newman-Keuls multiple comparisons of variance are significant (P < 0.01) when comparing Group 4 (ACS with stent) and Group 3 (ACS alone), and Group 4 (ACS with stent) and Group 2 (ACS with ELN section). It was not significant (P > 0.05) when comparing Group 2 (ELN section) and Group 3 (ACS alone).
12
Fig. 6. Ratio of subcricoid
Cricoid Area/lbcheal
Size
Control ACS-ELN
ACS
ACS
area to tracheal size. P -c 0.05 when comparing 3 (ACS alone) or 4 (ACS with stent).
Stent group 1 (Control) with groups
Fig. 7. Sectioning the subcricoid area demonstrated an elongation animals when the gap in the cricoid cartilage was small. A: control; alone; D: ACS with stent.
Fig. 8. Endoscopically
of the ventral dorsal axis in some B: ACS with ELN section; C: ACS
the gap in the cricoid cartilage (between arrows) resulted The true vocal cords (VC) are seen laterally.
in an enlarged
airway.
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When the ratio of cricoid gap divided by tracheal size is utilized, a one-way analysis of variance shows that F3,32 = 11.7. Newman-Keuls multiple comparisons were similar (P < 0.01) to the analysis for the ratio of gap divided by weight except a comparison between Group 3 (ACS) and Group 4 (ACS with stent) was no longer significant (P > 0.05). Ratios of the subcricoid area divided by the tracheal size showed Group 1 with a mean of 8.4 and a standard deviation (S.D.) of 1.5, Group 2 with a mean of 9.3 and a S.D. of 1.0, Group 3 with a mean of 9.8 and a S.D. of 0.8, and Group 4 with a mean of 10.2 and a S.D. of 1.5 (Fig. 6). Compared to controls, the subcricoid area for Group 2 increased ll%, for Group 3 178, and for Group 4 21%. A one-way multiple comparisons analysis of variance shows that I;3,32 - 3.18. Newman-Keuls are significant (P < 0.5) when comparing Group 1 (control) with either Group 3 (ACS alone) or with Group 4 (ACS with stent), but are not significant (P > 0.05) when making other group comparisons. The gross examination of the sections taken through the subcricoid area demonstrated a tendency toward an elongation of the airway in the ventral dorsal axis which is particularly evident when a small gap was present (Fig. 7). Whether this has an effect on airflow was not determined
Fig. 9. Histologic evaluation demonstrates the first tracheal ring underlying the cricoid cartilage due to shrinkage artifact. The gap in the cricoid cartilage is filled with fibroconnective tissue. A: control; B: ACS with ELN section; C: ACS alone; D: ACS with stent.
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Endoscopic examination did not demonstrate any narrowing or granulation tissue. When there was a significant cricoid gap the subglottic airway appeared to be enlarged (Fig. 8). Histologic evaluation of control animals shows a normal shape of the cricoid cartilage. The first tracheal ring underlies the cricoid cartilage which was not the state prior to fixation (Fig. 9). Evaluation of animals in experimental Groups 2, 3, and 4 shows that the gap in the cricoid cartilage is filled with fibroconnective tissue. As with the control group, the first tracheal ring underlies the cricoid cartilage which is attributed to fixation artifact. In no instance was there any evidence of polyps, granulation tissue, or submucosal cysts. One animal from Group 4 (ACS with stent) had significant aspiration problems postoperatively due to a rostral placement of the endotracheal tube and was euthanized. Measurements from this animal were not included in the results.
Discussion The pathophysiology of the ACS is poorly understood. Hollinger postulated 3 possible methods by which the ACS allows the patient to be extubated: (1) interruption of the cricoid ring releases compression of the soft tissue between the endotracheal tube and the cartilage thereby allowing restoration in circulation and resolution of edema and granulation tissue, (2) the cricoid cartilage gap allows an increase in the cross-sectional area of the subglottic lumen, (3) incision of the cartilage and mucosa allows tissue drainage of edema fluid and submucosal cysts
PI*
The results show that the ACS with a stent does, in fact, increase the subcricoid area. In Group 4 which underwent the ACS operation with the stent, there was a 21% increase in subcricoid area (Fig. 6). These results substantiate the findings by Babyak et al. which showed a 26% increase in size measured at the time of stent removal in 4 animals. In the non-diseased canine model, the ACS may be used to increase the subcricoid size. The use of the stent does have a positive effect on increasing the subglottic size. The animals with the stent had a greater increase in the cricoid gap (5.1 versus 2.6) and had a greater increase in the subcricoid area (21% versus 17%) (Figs. 5 and 6). In looking closely at the data (Table I) the stent does not result in an increase in the area in all animals. Rather, the use of the stent appears to eliminate cases in which there may have been a very minimal increase with the ACS procedure alone. This suggests that the use of the stent better guarantees an increase in the subglottic space by increasing the cricoid gap in animals that may have a minimal response to the ACS procedure. A seemingly small increase in the subglottic area may be quite significant clinically. With constant pressure, the flow through a pipe increases in proportion to the increase in the cross-sectional area. Clinically, an increase in the subglottic size of 21% may allow a child to be decannulated or extubated.
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Fig. 10. The effect of the cricothyroid and lateral cricoarytenoid and lateral cricoarytenoid muscle on the cricoid gap. A: at rest; B: with coughing or deep respirations the cricoid gap enlarges.
As the gap in the cricoid cartilage is much larger than the gap initially induced by the stent, this further supports our hypothesis that a stent may be irritating the larynx causing an increase in the muscular activity of the cricothyroid or the lateral cricoarytenoid muscle. Anatomically, one would expect that the cricothyroid muscle and the lateral cricoarytenoid muscles may both potentially cause a gap in the cricoid cartilage after the ACS procedure. Based on the location, direction of pull, and ability of the arytenoid to rotate when being pulled upon by the lateral cricoarytenoid muscle, the cricothyroid muscle should have the greater effect. The role the cricothyroid muscle plays on the ACS is not clear. Acutely, at the time of surgery, the cricothyroid muscle was found to have a strong effect on the gap in the cricoid cartilage which is greatly increased when the level of anesthesia was lightened (Fig. 10). With deep respirations, there was a marked gap in the cricoid cartilage upon expiration. Sectioning the external laryngeal nerve which innervates the cricothyroid muscle eliminated this gapping. These intraoperative findings strongly suggest that the cricothyroid muscle can play a dominant role in the outcome of the anterior cricoid split. Analyzing the long-term effects of sectioning the external laryngeal nerve was complicated by significant variability within each group. Sectioning of the external laryngeal nerve resulted in a smaller cricoid gap (2.6 mm vs 1.2 mm) and a smaller increase in the subcricoid area (17% vs 11%) (Figs. 5 and 6). As there was significant variability within the groups, these increases were not statistically significant (P > 0.05). This is not to say that the external laryngeal nerve does not produce a significant effect on the anterior cricoid split, but rather, statistically a conclusion could not be drawn regarding the long-term effects of the external laryngeal nerve section. It is likely that all or some of the factors suggested by Holinger may play a role when the ACS operation is successful. The current results suggest that in the canine model, the gap formation in the cricoid cartilage may play a significant role. Further, these results suggest that the neuromuscular activity of the cricothyroid muscle may play an important role in our active, non-sedated puppies, while other factors may be more important in the paralyzed or heavily sedated premature infant.
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Acknowledgements We thank the Genetics Committee of the Australian Shepherd Club of America for their support in this project; Maggie Chiu, Staff Research Associate, for her histologic help; and Laura Roberts who prepared the manuscript.
References 1 Babyak, J.W., Passamani, P.P. and Sullivan, M.J., The anterior cricoid split in puppies, Int. J. Pediat. Otolaryngol., 13 (1987) 191-204. 2 Cotton, R.T. and Seid, A.B., Management of the extubation problem in the premature child. Anterior cricoid split as an alternative to tracheotomy, Ann. Otol. 89 (1980) 508-511. 3 Frankel, L.R., Anas, N.G., Perkin, R.M., Seid, A.B., Peterson, B. and Park, S.M., Use of the anterior cricoid split operation in infants with acquired subglottic stenosis, Crit. Care Med. 12 (1984) 395-398. 4 Grundfast, K.M., Coffman, A.C. and Milmoe, G., Anterior cricoid split: a simple surgical procedure and a potentially complicated care problem, Ann. Otol., 94 (1985) 445-449. 5 Holinger, L.D., Stankiewicz, J.A. and Livingston, G.L., Anterior cricoid split: the Chicago experience with an alternative to tracheotomy, Laryngoscope, 97 (1987) 19-24. 6 Methods for connective tissue. In Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology, MC Graw-Hill, New York, 1960, p. 77. 7 Miller, R.H. and Weatherly, R.A., Experience with anterior cricoid split for difficult neonatal extubation, Arch. Otolaryngol. Head Neck Surg., 112 (1986) 972-975. 8 Pashley, N.R., Anterior cricoidotomy for congenital and acquired subglottic stenosis in infants and children, J. Otol., 13 (1984) 187-190. 9 Seid; A.B. and Canty, T.G., The anterior cricoid split procedure for the management of subglottic stenosis in infants and children, J. Pediat. Surg., 20 (1985) 388-390. 10 Senders, C.W. and Eisele, P.H., The anterior cricoid split explored via the canine model, preliminary studies, Int. J. Pediat. Otolaryngol., 14 (1988) 175-185.