Abstract
Objectives
The aim of this study was to evaluate two unilateral laryngoplasty (arytenoid lateralisation) techniques for use in the surgical management of laryngeal paralysis in cats.
Methods
Left cricoarytenoid abduction (lateralisation) was performed in 20 ex vivo cat larynges; 10 following complete cricoarytenoid disarticulation (group LAA-dis) and 10 following no cricoarytenoid disarticulation (group LAA-nodis). For both groups, left arytenoid abduction (LAA) was measured in the resting and postoperative larynges using image analysis software. Measurements were evaluated using the Mann–Whitney U-test. For both groups, dorsal images of the postoperative larynges were assessed visually for evidence of epiglottic coverage of the entrance to the larynx.
Results
The mean percentage increase in LAA was 311.5% and 199.4% (P <0.006) for group LAA-dis (complete cricoarytenoid disarticulation) and group LAA-nodis (no cricoarytenoid disarticulation), respectively. In both groups, there was no evidence of a lack of epiglottic coverage of the entrance of the larynx for any of the postoperative larynges.
Conclusions and relevance
Placement of a single, tensioned suture between the muscular process of the left arytenoid cartilage and the caudolateral aspect of the ipsilateral cricoid cartilage (unilateral cricoarytenoid lateralisation) resulted in abduction of the left arytenoid cartilage and a corresponding increase in the area of the rima glottidis on the operated side. The clinical significance of the difference in outcome between left cricoarytenoid abduction following complete cricoarytenoid disarticulation and abduction following no cricoarytenoid disarticulation remains unclear, and both might be considered appropriate for the surgical management of laryngeal paralysis in the cat.
Introduction
Laryngeal paralysis is an uncommon cause of upper airway obstruction in the cat. Although the condition is well recognised in dogs, it is much less frequently reported in cats.1–12
The condition is reported to occur most frequently in middle-aged to older cats (mean age 9–14 years), and the paralysis may be both unilateral and bilateral in presentation, although in the relatively small number of cases reported there appears to be a prevalence of left-sided unilateral paralysis similar to that reported in horses and people. 13 Importantly, unlike the condition in dogs, unilateral paralysis in cats can result in significant and life-threatening clinical signs.1,6–8
In the cat, although several causes have been reported, including trauma, neoplastic invasion and iatrogenic damage, the aetiology in most cases remains undetermined, and the condition is categorised as idiopathic in nature. 13
Conservative management of the condition in cats consists of weight loss and minimising excitement and rigorous exercise. 13 The severity of clinical signs and the poor response to conservative management indicate a requirement for surgical intervention in many individuals, both those affected bilaterally and those affected by unilateral paralysis. Reported surgical procedures in the cat include partial laryngectomy with vocal fold removal; castellated laryngofissure, including vocal fold removal; arytenoid cartilage lateralisation (unilateral or bilateral); and permanent tracheostomy.2,3,5–8,10 In cats, although only a small number of cases have been reported, it is generally agreed that unilateral arytenoid abduction (lateralisation) represents the preferred surgical procedure for both unilateral and bilateral laryngeal paralysis.13–15
Similar to the dog, the aim of surgical treatment is to increase the area of the rima glottidis. 16 Although such surgeries will alleviate the clinical signs of airway obstruction, they are also associated with a number of potential serious complications, including aspiration pneumonia, laryngeal webbing, surgical failure, seroma formation at the surgical site, airway re-obstruction secondary to laryngeal oedema and transient Horner’s syndrome. 14 In clinical cases of bilateral laryngeal paralysis in the dog, various modifications of the unilateral arytenoid lateralisation procedure have been reported, including cricoarytenoid, thyroarytenoid and a combination of cricoarytenoid/thyroarytenoid lateralisation.17–19 In addition, studies have reported the effects of modifications to the arytenoid lateralisation procedure in cadaveric canine larynges.16,20,21 The overall aim of such studies is to define the most effective surgical management for laryngeal paralysis that is associated with the minimal number of complications.
Currently, in the cat there are no studies investigating similar modifications to the ‘standard’ arytenoid lateralisation procedure described previously.6,8 The aim of this study was to document and compare the percentage increase in arytenoid cartilage abduction in ex vivo cat larynges on which two modifications of the unilateral arytenoid lateralisation surgical procedures were performed. In addition, for both surgical procedures, an assessment of epiglottic coverage of the entrance to the larynx was performed.
Materials and methods
The tongue, larynx, cervical trachea and oesophagus were harvested en bloc from 20 mature domestic shorthair cats euthanased for reasons unrelated to this study. None of the cats was euthanased for reasons of respiratory disease or respiratory compromise. All larynges appeared anatomically normal. They were washed and wrapped in saline soaked swabs (0.9% NaCl) before being stored at −18°C. All larynges were used within 4 weeks of harvest and frozen storage. On the day of study, the larynges were allowed to defrost and warm to room temperature before being further washed in room temperature normal saline. The tongue and oesophagus were resected from each larynx prior to obtaining any measurements or performing any surgical intervention. A stay suture of 4/0 polypropylene (Prolene; Ethicon) was inserted through the tip of the epiglottis, and both suture ends were clamped in the jaws of a pair of Halstead mosquito forceps to allow manipulation of the epiglottis. A 0.3 mm diameter pin (Watkins and Doncaster) was inserted through the thyroid cartilage on the ventral floor of the rima glottidis, in the midline between the insertion of the left and right vocal folds so that its tip and shaft indicated the ventral bisection of the rima glottidis into left and right halves.
A rig was constructed that allowed each larynx to be positioned in a consistent and repeatable manner. A single reflex digital camera (Canon EOS 5D Mark IV; Canon Europa) with an attached micro lens (Canon EF 100 mm f2.8 USM Macro Lens; Canon Europa) was positioned in linear alignment with a 4.8 mm diameter Steinmann pin (Veterinary Instrumentation). Prior to obtaining images, the distal tracheal end of the tissue specimen was slid onto the end of the Steinmann pin. In each case, the pointed tip of the pin was positioned at the level of the caudal aspect of the ventral aspect of the thyroid cartilage. This ensured that the sample was consistently in linear alignment with the camera’s lens and digital sensor. Positioning the tip of the pin at this level ensured that the pin itself had no influence on the resting position of the arytenoid cartilages. A reticle with a 1 mm scale subdivided into 10 divisions of 0.1 mm (Reticle Calibration Slide; Muhwa Scientific) was placed dorsal to the larynx at the level of the cranial aspect of the arytenoid and was included in all images obtained. The 0.1 mm graduations provided a scale for calculating the lateralisation of the operated arytenoid cartilage. Images were recorded and stored to a digital memory card (SanDisk 128 GB Extreme Pro SDXC card). Images were obtained of each larynx before and after unilateral surgical abduction of the arytenoid cartilage.
Using a computer-generated random numbers table, the 20 larynges were randomly assigned to one of two groups: group LAA-dis (n = 10; unilateral arytenoid abduction with disarticulation of the arytenoid from the cricoid); and group LAA-nodis (n = 10; unilateral arytenoid abduction with no disarticulation of the arytenoid from the cricoid). All surgeries were performed by the same board-certified surgeon.
Figure 1 shows the normal relationship of the laryngeal cartilages from the left side for reference. Left-sided ary-tenoid abduction was performed using the following techniques. In both groups, the thyropharyngeus muscle on the left side was incised transversely along a line adjacent to the dorsal aspect of the wing of the underlying thyroid cartilage, revealing the cricothyroid articulation. 6 Using a number 11 scalpel blade, the thyroid cartilage was disarticulated from the cricoid cartilage. A stay suture of 4/0 polypropylene with a ½ curved 17 mm taper-cut needle (W8935 Prolene; Ethicon) was placed through the dorsal aspect of the left wing of the thyroid cartilage allowing the cartilage to be reflected laterally. 6
Normal relationship of the laryngeal cartilages from the left side, for reference
In the LAA-dis group, the muscular process of the arytenoid was recognised and the insertion of the dorsal cricoarytenoideus muscle was sectioned. A number 11 blade was used to incise the joint capsule of the cricoarytenoid articulation. The incision was extended around the entire capsule resulting in the complete disarticulation of the left arytenoid cartilage from the left cricoid cartilage. 6 A 5/0 polypropylene suture with a ½ curved 17 mm taper-cutting needle (VP-934-X Surgipro II; Covidien) was passed through the caudolateral aspect of the cricoid dorsal to the transected cricothyroid articulation (Figure 2). This suture was then looped around the caudal aspect of the arytenoid cartilage (to include at the site of the insertion of the dorsal cricoarytenoideus muscle) by passing the suture twice through the articular facet on the medial aspect of the arytenoid cartilage (Figures 3 and 4). The suture was then passed through the caudolateral aspect of the cricoid for a second time (Figure 5) before the suture was tensioned (tightened until resistance was appreciated) and tied (Figure 6). 22 A single interrupted suture of 5/0 polypropylene was passed through the caudolateral aspect of the cricoid, exiting the cricoid through the cricothyroid articulation, before being passed through the thyroid via the cricothyroid articulation. By tying this suture, the anatomical integrity of the cricothyroid articulation was re-established (Figure 7).
Placement of the cricoarytenoid abduction suture through the caudolateral aspect of the cricoid dorsal to the transected cricothyroid articulation
Cricoarytenoid abduction suture being passed through the caudal aspect of the arytenoid cartilage to include at the site of the insertion of the dorsal cricoarytenoideus muscle and the articular facet on its medial aspect
Cricoarytenoid abduction suture being passed through the caudal aspect of the arytenoid cartilage for a second time to create a suture loop
Cricoarytenoid abduction suture being passed through the caudolateral aspect of the cricoid for a second time
Suture being tensioned and tied
Integrity of the cricothyroid articulation was re-established by passing a suture through the caudolateral aspect of the cricoid, which then exited the cricoid through the cricothyroid articulation before being passed through the thyroid via the cricothyroid articulation
In the LAA-nodis group, the muscular process of the arytenoid was recognised, but the insertion of the dorsal cricoarytenoideus muscle and the joint capsule of the cricoarytenoid articulation were left intact. Similar to the LAA-dis group, a 5/0 polypropylene suture was passed through the caudolateral aspect of the cricoid dorsal to the transected cricothyroid articulation before being looped around the caudal aspect of the arytenoid cartilage (to include at the site of the insertion of the dorsal cricoarytenoideus muscle) by passing the suture twice through this aspect of the cartilage. Similar to the LAA-dis group, the suture was then passed through the caudolateral aspect of the cricoid for a second time before the suture was tensioned and tied. The cricothyroid joint was repaired in a similar manner to that described for the LAA-dis group.
For both groups (post-arytenoid abduction surgery), a further digital photograph of the dorsal larynx was obtained following manipulation of the epiglottis into its closed position using the previous placed stay suture. These images were reviewed by both authors for evidence of a lack of epiglottic coverage of the entrance to the larynx (Figure 8). 16
Postoperative dorsal larynx of cat 18 obtained following manipulation of the epiglottis into its closed position using the epiglottic stay suture. The image shows no evidence of a lack of laryngeal epiglottic–glottic seal
Pre- and postoperative images for both groups were uploaded onto a computer. Using presentation software (PowerPoint; Microsoft), a line was drawn that bisected the rima glottidis in the dorsoventral midline. A second line was drawn perpendicular to this at a point where it contacted the medial aspect of the mucosa covering the caudal limit of the left arytenoid cartilage (Figure 9). The distance of arytenoid abduction (pre- and postoperatively for both groups) was measured using ImageJ (National Institutes of Health). Calibration was accomplished using the 0.1 mm scale included on each image. The values of these measurements were used to calculate the percentage increase in abduction for each larynx in both groups.
(a) Preoperative image of cat 18 showing the rima glottidis and reticle scale. A line has been drawn to bisect the rima glottidis in the dorsoventral midline. A second line has been drawn perpendicular to this at a point where it contacted the medial aspect of the mucosa covering the caudal limit of the left arytenoid cartilage. This distance represents the length of left arytenoid abduction (LAA) in the resting larynx. Note the asymmetry in the resting positions of the left and right arytenoid cartilages. (b) Postoperative image of the same larynx (cat 18) showing the rima glottidis, reticle scale and lines allowing for measurement of the length of LAA following surgical intervention
The data were tested for normality using a Kolmogorov–Smirnov test. Further statistical analysis of the data was performed using the Mann–Whitney U-test to compare the percentage increase in arytenoid abduction values between the two surgical groups. Statistical significance was accepted at P <0.05. Statistical analysis was undertaken using GraphPad Prism 9.4.0 for MacOS.
Results
The distance and percentage increases in abduction measurements are presented in Table 1.
Left arytenoid abduction (LAA) measurements with and without disarticulation
M = male; F = female
The Kolmogorov–Smirnov test confirmed that the data were normally distributed. For the LAA-dis group, the mean ± SD percentage increase in abduction was 311.5 ± 88.4, while for the LAA-nodis group, it was 199.4 ± 64.6. This difference was statistically significant (P <0.006). These data are presented as a box plot in Figure 10.
Box plot showing the range and mean percentage increase in left arytenoid abduction for ex vivo cat larynges undergoing left cricoarytenoid abduction either following complete cricoarytenoid disarticulation (arytenoid disarticulation) or following no cricoarytenoid disarticulation (no arytenoid disarticulation)
Neither observer recorded evidence of a lack of epiglottic coverage of the entrance of the larynx for any of the postoperative larynges in either group.
Discussion
The findings of this study indicate that placement of a single tensioned suture between the muscular process of the left arytenoid cartilage and the caudolateral aspect of the ipsilateral cricoid cartilage (unilateral cricoarytenoid lateralisation) resulted in abduction of the left arytenoid cartilage and a corresponding increase in the area of the rima glottidis on the operated side. The findings also indicate that unilateral arytenoid lateralisation following the complete disarticulation of the left arytenoid cartilage (LAA-dis) resulted in significantly greater abduction of the left arytenoid cartilage compared with lateralisation following no arytenoid disarticulation (LAA-nodis).
The role of extraluminal surgical techniques in the management of laryngeal paralysis is to anchor one of the arytenoid cartilages in its abducted position and, as a consequence, increase the area of the rima glottidis during the inspiratory phase of respiration. In the dog, a number of previous experimental and in vivo studies investigating the effects of various modifications to the arytenoid lateralisation technique have been described.16,18,19,22–28 In general, these have used the area of rima glottidis as an outcome measurement for each technique’s effectiveness.16,18–20,23,28
For consistency of study design, in this study, attempts were made to use the area of the rima glottidis as an outcome measurement. Such measurements proved unreliable in the ex vivo cat larynx for the following reasons. First, it was found that there was often an inconsistency and asymmetry in the resting positions of the arytenoid cartilages in the larynges. This variation and asymmetry made the use of resting rima glottidis area data both unreliable and untrustworthy. In addition, visualisation of the entire circumference of the rima glottides, while maintaining orientation of the linear alignment of the camera lens, required excessive cranioventral traction on the tip of the epiglottis (using the preplaced stay suture). Such traction resulted in an obvious change in the resting positions of both the left and right arytenoid cartilages making this procedure similarly unreliable. As a result of these inconsistencies, the measurement of the pre- and postoperative LAA was used to assess the effectiveness of the two techniques in their ability to increase the size of the rima glottidis.
In this study, the ex vivo larynges were stored at −18°C before being defrosted and washed in room temperature normal saline prior to surgical manipulation. In previous studies performed in the dog, a number of storage strategies for ex vivo larynges have been described. These include the use of: fresh harvested larynges; 23 fresh larynges that were stored in saline-soaked swabs at 2°C for 24 h 29 or up to a week before the study; 22 larynges fixed in 2-phenoxyethanol 2%, wrapped in saline-soaked swabs and stored at 4°C for up to 2 weeks before the study;19,20 larynges harvested after storing the complete cadaver at 5°C for up to 48 h before the study; 30 or larynges stored at −20°C for use within 1 day after thawing. 21 Although not studied specifically, Guillemot et al suggested that fixing ex vivo larynges with 2-phenoxyethanol 2% prior to storage preserved soft tissue properties while maintaining the mobility of the arytenoid cartilages. 21 In the current study, no investigations were undertaken to determine if the storage regime had a negative impact on soft tissue properties. It might be argued that the inconsistency and asymmetry in the resting positions of the left and right arytenoid cartilages observed in the study were a result of the frozen storage regime. We accounted for this discrepancy of resting arytenoid position by using the abduction of the left arytenoid rather than the area of the rima glottidis as the outcome assessment of the two surgical techniques. Regardless, and similar to a previous study in dogs, frozen storage of the larynges did not appear to affect the dynamic mobility of the left arytenoid cartilage and no problems were encountered abducting the arytenoid cartilages when performing either of the two procedures. 21
To our knowledge, no previous studies have investigated the specific effects of the arytenoid lateralisation technique on either the rima glottidis area or degree arytenoid abduction in the cat. Previous reports describing arytenoid lateralisation in the cat are all retrospective clinical case series.5–10 Within these studies, the description of the surgical technique was mostly non-specific and poorly described. Despite this, the studies indicated that a wide range of lateralisation techniques were performed, including cricoarytenoid lateralisation, thyroarytenoid lateralisation and combined cricothyroarytenoid lateralisation – with variation in the concurrent use of cricothyroid, cricoarytenoid (partial or complete) and interarytenoid disarticulation.5–10
The results of this study – which indicate that unilateral arytenoid lateralisation following LAA-dis results in significantly greater abduction of the left arytenoid cartilage when compared with LAA-nodis – are at odds with previous reports in dogs.16,20 In the dog, studies suggest that the disarticulation of the arytenoid cartilage from the cricoid cartilage has no effect on the ability of the lateralisation surgery to increase the area of the rima glottidis vs the procedure being performed on a larynx without disarticulation of the arytenoid cartilage.16,20 Despite this lack of difference, partial disarticulation of the cricoarytenoid joint is considered to allow for safer placement of the cricoarytenoid suture, reducing the possibility of cartilage fracture.14–16,23,31 In the dog, differences in surgical technique and the degree of increase in surface area of the rima glottidis do not seem to affect postoperative clinical signs and outcome. 13 However, increasing the surface area of the rima glottidis beyond the edges of the epiglottis is considered to put the animal at a higher risk of aspiration.13,16 Studies also indicate that limited lateral displacement of the arytenoid cartilage can significantly reduce resistance to airflow within the larynx while at the same time potentially decreasing the risk of postoperative aspiration. 21 It has been suggested that this limited, but effective, lateral displacement of the arytenoid cartilage can be accomplished by minimising the degree of laryngeal dissection; that is, by not performing cricothyroid disarticulation, interarytenoid disarticulation or complete disarticulation of the cricoarytenoid articulation. 13
In cats, postoperative aspiration pneumonia is a well-recognised complication of arytenoid lateralisation surgery for the management of laryngeal paralysis, and this might be related to the degree of arytenoid abduction achieved at the time of lateralisation surgery. 8 If this were the case, there might be an argument that limited laryngeal dissection – that is, only partial rather than full disarticulation of the cricoarytenoid joint – might be the preferred surgical technique. Further objective studies in cats suffering from laryngeal paralysis are required to ascertain whether the greater abduction achieved by complete disarticulation of the left arytenoid cartilage results in a better or worse clinical outcome than lateralisation surgery without disarticulation of the arytenoid cartilage. Regardless, the results of this study suggest that there is likely to be no requirement for, or benefit from, the disarticulation of one arytenoid cartilage from the other. Further studies are required to assess the effect and requirement for disarticulation of the cricothyroid articulation when performing arytenoid lateralisation surgery in cats suffering from laryngeal paralysis.
Previous studies in dogs have attempted to assess the effect of unilateral arytenoid lateralisation on laryngeal epiglottic–glottis seal.21,23 In this study, an attempt was made to replicate previously reported methods for pulling the epiglottic cartilage into its closed position. In the dog, this has been achieved by the placement of a stay suture through the mucosa at the tip of the rostral point of the epiglottis with this suture then being passed through the rima glottidis and the tracheal lumen. 23 Traction on the suture caused the epiglottis to move from its open resting position to a closed position covering the opening to the larynx. When this method was attempted in the cat, the flexible and elastic nature of the epiglottic cartilage caused the structure to deform and fold along its longitudinal axis. As a result, the method for moving the cartilage into its closed position was modified in such a way that the stay suture was pulled in a caudal direction from outside the tracheal lumen rather than from within. Since this modified method of closure was considered non-physiological, and also open to bias (excessive dorsal traction), the findings of epiglottic closure were restricted to a simple visual assessment of whether the arytenoid lateralisation resulted in a gap between the dorsolateral aspect of the epiglottis and the arytenoid cartilage on the operated side.
The authors recognise that their experimental design is open to both conscious and unconscious bias; for example, all surgical procedures were undertaken by the same individual, there was no blinding of the experimental data and the sample size was small making it unsafe to infer any firm conclusions from the data analysis. We acknowledge these limitations and their effects on the validity, reliability and interpretation of the study’s results. Future studies might consider the use of a tension meter when tying the abduction suture in an attempt ensure consistency in suture tension and to reduce bias in this aspect of the study design.
Conclusions
This study indicates that placement of a single, tensioned suture between the muscular process of the left arytenoid cartilage and the caudolateral aspect of the ipsilateral cricoid cartilage (unilateral cricoarytenoid lateralisation) resulted in abduction of the left arytenoid cartilage and a corresponding increase in the area of the rima glottidis on the operated side. The clinical significance of the difference in outcome between LAA-dis and LAA-nodis remains unclear, and both might be considered appropriate for the surgical management of laryngeal paralysis in the cat.
Footnotes
Conflict of interest
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Ethical approval
The work described in this manuscript involved the use of non-experimental (owned or unowned) animals. Established internationally recognised high standards (‘best practice’) of veterinary clinical care for the individual patient were always followed and/or this work involved the use of cadavers. Ethical approval from a committee was therefore not specifically required for publication in JFMS. Although not required, where ethical approval was still obtained, it is stated in the manuscript.
Informed consent
Informed consent (verbal or written) was obtained from the owner or legal custodian of all animal(s) described in this work (experimental or non-experimental animals, including cadavers) for all procedure(s) undertaken (prospective or retrospective studies). No animals or people are identifiable within this publication, and therefore additional informed consent for publication was not required.
