Ex vivo modeling of the airflow dynamics and two-and three-dimensional biomechanical effects of suture placements for prosthetic laryngoplasty in horses

Nicola P. Lynch 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Sarah A. Jones 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Lucy G. Bazley-White 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Zoe F. Wilson 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Jennifer Raffetto 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Thilo Pfau 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Jonathon Cheetham 2Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Justin D. Perkins 1Department of Veterinary Clinical Sciences, Royal Veterinary College, University of London, North Mymms, Herfordshire, AL9 7TA, England.

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Abstract

OBJECTIVE

To identify the degree of left arytenoid cartilage (LAC) abduction that allows laryngeal airflow similar to that in galloping horses, assess 2-D and 3-D biomechanical effects of prosthetic laryngoplasty on LAC movement and airflow, and determine the influence of suture position through the muscular process of the arytenoid cartilage (MPA) on these variables.

SAMPLE

7 equine cadaver larynges.

PROCEDURES

With the right arytenoid cartilage maximally abducted and inspiratory airflow simulated by vacuum, laryngeal airflow and translaryngeal pressure and impedance were measured at 12 incremental LAC abduction forces (0% to 100% [maximum abduction]) applied through laryngoplasty sutures passed caudocranially or mediolaterally through the left MPA. Cross-sectional area of the rima glottis and left-to-right angle quotient were determined from photographs at each abduction force; CT images were obtained at alternate forces. Arytenoid and cricoid cartilage markers allowed calculation of LAC roll, pitch, and yaw through use of Euler angles on 3-D reconstructed CT images.

RESULTS

Translaryngeal pressure and impedance decreased, and airflow increased rapidly at low abduction forces, then slowed until a plateau was reached at approximately 50% of maximum abduction force. The greatest LAC motion was rocking (pitch). Suture position through the left MPA did not significantly affect airflow data. Approximately 50% of maximum abduction force, corresponding to a left arytenoid angle of approximately 30° and left-to-right angle quotient of 0.79 to 0.84, allowed airflow of approximately 61 ± 6.5 L/s.

CONCLUSIONS AND CLINICAL RELEVANCE

Ex vivo modeling results suggested little benefit to LAC abduction forces > 50%, which allowed airflow similar to that reported elsewhere for galloping horses.

Abstract

OBJECTIVE

To identify the degree of left arytenoid cartilage (LAC) abduction that allows laryngeal airflow similar to that in galloping horses, assess 2-D and 3-D biomechanical effects of prosthetic laryngoplasty on LAC movement and airflow, and determine the influence of suture position through the muscular process of the arytenoid cartilage (MPA) on these variables.

SAMPLE

7 equine cadaver larynges.

PROCEDURES

With the right arytenoid cartilage maximally abducted and inspiratory airflow simulated by vacuum, laryngeal airflow and translaryngeal pressure and impedance were measured at 12 incremental LAC abduction forces (0% to 100% [maximum abduction]) applied through laryngoplasty sutures passed caudocranially or mediolaterally through the left MPA. Cross-sectional area of the rima glottis and left-to-right angle quotient were determined from photographs at each abduction force; CT images were obtained at alternate forces. Arytenoid and cricoid cartilage markers allowed calculation of LAC roll, pitch, and yaw through use of Euler angles on 3-D reconstructed CT images.

RESULTS

Translaryngeal pressure and impedance decreased, and airflow increased rapidly at low abduction forces, then slowed until a plateau was reached at approximately 50% of maximum abduction force. The greatest LAC motion was rocking (pitch). Suture position through the left MPA did not significantly affect airflow data. Approximately 50% of maximum abduction force, corresponding to a left arytenoid angle of approximately 30° and left-to-right angle quotient of 0.79 to 0.84, allowed airflow of approximately 61 ± 6.5 L/s.

CONCLUSIONS AND CLINICAL RELEVANCE

Ex vivo modeling results suggested little benefit to LAC abduction forces > 50%, which allowed airflow similar to that reported elsewhere for galloping horses.

Recurrent laryngeal neuropathy is a performance-limiting disease in equine athletes. Primary axonal dysfunction, predominantly of the left recurrent laryngeal nerve, results in laryngeal dysfunction through the loss of cricoarytenoideus dorsalis muscle function.1 The unilateral loss of arytenoid cartilage abduction results in reduced CSA of the rima glottidis, reduced inspiratory airflow, and increased inspiratory resistance.2,3 Various surgical treatment options for recurrent laryngeal neuropathy have been described, including prosthetic laryngoplasty, arytenoidectomy, ventriculocordectomy alone or in combination with prosthetic laryngoplasty, and modified first or second cervical nerve graft.4–10 Prosthetic laryngoplasty as first described by Marks et al4 remains the most commonly used technique for the treatment of recurrent laryngeal neuropathy. The standard technique is performed by placement of a suture between the MPA and cricoid cartilage, 2 to 3 cm cranial the caudal border of the cricoid cartilage.11 On the basis of computational modeling and results of in vivo studies, the recommended amount of arytenoid cartilage abduction is 80% to 90% of maximum CSA in racehorses and 60% to 80% in horses that do not routinely undergo intense exercise.12,13 Postoperative complications associated with laryngeal dysfunction and potentially linked to excessive abduction include coughing, excessive tracheal mucus production, nasal discharge, dysphagia, and aspiration pneumonia, and the risk of these complications may offset the benefits of near-maximum abduction.14

Several studies15–19 have focused on techniques to reduce the risk of prosthesis failure after laryngoplasty through selection of stronger suture material and altered placement of the suture through the MPA and the cricoid cartilage15–19 and have evaluated the effects of these changes on rima glottidis area measurements.18,19 Results of some studies16,20 indicate that suture placement oriented to the fiber direction of the lateral neuromuscular compartment of the cricoarytenoideus dorsalis muscle provides optimal arytenoid cartilage abduction. Moreover, application of 2 sutures further improves the degree of abduction, regardless of the orientation of the prosthesis between the cricoid cartilage and the MPA.13,16,18,20,21 To the authors' knowledge, there have been no previous studies to compare the effect of altering prosthesis placement through the MPA on airflow and 3-D biomechanics of the arytenoid cartilage.

The objectives of the study reported here were to identify the degree of arytenoid cartilage abduction required to establish laryngeal airflow measurements similar to those identified in galloping or maximally exercising horses (56 to 76 L/s),3,22 investigate the 2-D and 3-D biomechanical effects of prosthetic laryngoplasty on arytenoid cartilage movement and the relationship of these effects to airflow, and determine the influence of suture position through the MPA on these variables in an ex vivo model.

Materials and Methods

Specimen preparation and prosthetic laryngoplasty

Seven larynges were obtained from the cadavers of horses that measured ≥ 162.5 cm in height at the highest point of the shoulders (ie, withers). Breed, sex, and age of the animals were unknown. All specimens were inspected by 1 author (JDP) to ensure there was no macroscopic pathology evident and were placed in 2% 2-phenoxyethanol preservative solution and stored at 4°C to maintain tissue pliability until use. The larynges were allowed to reach room temperature prior to testing.

The extrinsic musculature and the cricoarytenoideus dorsalis muscles were carefully removed to ensure the cricoarytenoid joint and its ligamentous attachments were retained intact on the specimen. Tracheal rings were removed except for the 2 most rostral rings, which were required for mounting. Each larynx was secured to a wooden mounting board by placing a 0.5-cm-diameter plastic bolt through the cricothyroid ligament. Four stay sutures of 0.65-mm nylon monofilamenta were used to prevent rotation of the larynx during force application. A suture was used to draw the epiglottic cartilage cranially so that the vocal folds were visible. The larynges remained secured to the mounting board for the duration of the experiments. Three radiopaque spherical 3-mm external markers were sutured to the following anatomic sites for use in CT analyses: the dorsal midline between the arytenoid cartilages, the left MPA (attachment for the cricoarytenoid dorsalis muscle), and a point one-third of the distance from the caudal notch of the cricoid cartilage to the right MPA (in a caudal-to-cranial direction) on each larynx. Specimens with similar caudal notches were selected to allow for consistent marker placement.

In all larynges, the right and left arytenoid cartilages were maximally abducted by use of a standard prosthetic laryngoplasty technique for placement of the suture through the cricoid cartilage.11 A 2-mm hole was drilled in the cricoid cartilage 1.5 cm lateral to the midline and 1.5 cm from the caudal edge before introducing USP size-1 braided polyester multifilament suture,b which was positioned through the right MPA in a mediolateral direction. Initially, the suture was placed through the left MPA in a caudocranial direction for all specimens (Figure 1). The free ends of the suture material were tied in a loop and attached to a portable force meter.c The force required to maximally abduct each arytenoid cartilage, defined as the force at which greater tension on the suture did not cause any further visible movement of the arytenoid cartilage, was recorded for each larynx. The suture for the right arytenoid cartilage was double clamped in place with artery forceps when maximum abduction force was reached; this remained static throughout the experiment.

Figure 1—
Figure 1—

Schematic diagram (dorsal view) of suture placements through the MPA in a study to identify the degree of arytenoid cartilage abduction required to create laryngeal airflow similar to that in galloping horses, assess 2-D and 3-D biomechanical effects of prosthetic laryngoplasty on arytenoid cartilage movement and airflow measurements, and determine the influence of suture position through the MPA on these variables in an ex vivo model. A = Arytenoid cartilage (corniculate process). Cr = Cricoid cartilage. FT = Force transducer. L = Left. R = Right. T = Trachea. Th = Thyroid cartilage.

Citation: American Journal of Veterinary Research 81, 8; 10.2460/ajvr.81.8.665

For the left arytenoid cartilage, the measurement of force required to achieve maximum abduction was divided into 12 equal sequential abduction force values between 0 N and the recorded maximum value. Airflow and 2-D and 3-D biomechanical testing was performed at 0 N and each of the predetermined abduction forces up to and including the previously determined maximum value for each larynx (ie, from 0% to 100% of maximum force in increments of 1/12 (approx 8.3%). Once all initial tests had been completed on each larynx, the left prosthetic laryngoplasty suture was removed and a new suture was placed with the same method through the cricoid cartilage. This suture was positioned through the MPA in a mediolateral direction, and results were recorded.

Differential pressure and air velocity measurement

An air velocity sensord was used to measure air velocity (in meters per second) through the larynx. A plastic catheter was incorporated into the housing surrounding the air velocity sensor and connected to a pressure transducere to measure differential TP (in centimeters of H2O). Plastic tubing connected the larynx to the differential pressure and air velocity sensor apparatus. This was inserted into the tracheal lumen and advanced as far cranially as possible to lie underneath the cricoid cartilage and then secured to the remaining tracheal rings with 0.65-mm nylon monofilament suture.a The sensor housing for the pressure transducer and the air velocity sensor consisted of an airtight fiberglass tunnel surrounding the air velocity sensor that tapered to the diameter of the larynx and had a smooth inner surface to reduce air turbulence. A vacuum cleanerf with a constant suction strength (280 airwatts) was attached to the tubing at the caudal end of the larynx and was used to simulate inspiratory airflow. The system was run for 10 seconds prior to obtaining readings. At 0 N and each of the subsequent abduction forces, 5 consecutive measurements were taken at 10-second intervals for air velocity and differential pressure measurements. The mean air velocity and differential pressure values over the 5 consecutive measurements were calculated at each force applied. Airflow (in liters per second) was calculated by multiplying air velocity by the area of the airflow apparatus. The TI (in centimeters of H2O per liter per second) was calculated as the quotient of TP divided by airflow.

2-D biomechanical modeling

A digital camerag was placed at a set distance of 60 cm from the tip of the epiglottis, and images of each larynx were taken at each abduction force applied for both mediolateral and caudocranial suture positions while the flow model was running. Arytenoid angles, LRQs, and CSA ratios for the rima glottis were measured from the imagesh at every abduction force used. The arytenoid angle and LRQ were calculated as described previously23 by drawing a vertical line connecting the most proximal and distal points of the rima glottis and extending this line proximally for a distance one-third of the dorsoventral height of the rima glottis. Tangenital lines to both of the arytenoid cartilages were drawn, and the angles between the dorsoventral line and the tangents were measured. The LRQ was obtained by dividing the right angle by the left angle. The CSA ratio was calculated by digitally tracing the lumen of the rima glottis initially as a whole with and without the vocal folds. The left and right CSAs were determined by digitally tracing the left and right halves of the rima glottis to a midway point defined by a vertical line extending distally from the midpoint of the corniculate cartilages. These were used to determine a left-to-right CSA ratio.

3-D biomechanical modeling

Laryngeal CT scans were performed with an 8-slice, fourth-generation CT scanner.i Images were obtained with a slice thickness and slice distance of 1.5 mm (120 kV and 100 mA) at alternate abduction forces (from approx 17% to 100%) for the caudocranial and mediolateral suture positions. Three-dimensional reconstructed images were created with grayscale thresholding for segmentation and subsequent surface wrapping by polynomial meshing.16 The coordinates of the center points for the 3 external markers (sutured into position as previously described) for each larynx were ascertained in each case. An additional marker at the junction of the arytenoid cartilage and the aryepiglottic fold was included as a reference point (ventral corniculate marker) in the software program,j and 2 additional virtual markers were plotted in the software programj in the same plane as the external marker that was sutured into place between the caudal notch of the cricoid cartilage and the MPA; one was placed directly dorsal and the other directly cranial to the original cricoid cartilage marker (Figure 2).

Figure 2—
Figure 2—

Representative 3-D reconstructed CT images (rostrocaudal [A] and left-to-right oblique [B] views) of the larynx from an equine cadaver with maximum arytenoid cartilage abduction created by prosthetic laryngoplasty. Markers were sutured at the dorsal midline between the arytenoid cartilages (AryMid), on the left MPA, and one-third of the distance from the caudal notch of the cricoid cartilage to the MPA; 2 additional virtual markers were plotted in the software programj in the same plane as the latter marker on the cricoid cartilage (one directly dorsal and the other directly cranial to the physical cricoid cartilage marker); the site of these 3 markers is shown (3Cric). The x-, y-, and z-axes are depicted as well as the rotations around these axes, representing pitch, yaw, and roll. Triangles depict the arytenoid cartilage markers (green) and the cricoid cartilage markers (red) used to calculate the rotation of the arytenoid markers relative to the cricoid cartilage. M4 = Radiopaque marker used to determine the position of the larynx relative to the CT scanner table. VenC = Ventral corniculate marker added as a reference point at the junction of the arytenoid cartilage and the aryepiglottic fold in the software.

Citation: American Journal of Veterinary Research 81, 8; 10.2460/ajvr.81.8.665

A fixed radiopaque marker was used to determine the fixed position of the larynx relative to the CT scanner table (Figure 2). The x-, y-, and z-coordinates for all the markers were determined, and translational movement of the larynx was compensated for by expressing the movement relative to the marker used to determine laryngeal position relative to the scanner table. The marker plotted dorsal to the original cricoid cartilage marker in the software was used as the origin of the Cartesian coordinate system, and the movements of the remaining markers were expressed relative to this designated origin (x-, y-, and z-axis origins of 0, 0, and 0). This was calculated by subtracting the coordinates of each marker at a force of 0 N from its respective coordinates at each subsequently applied force. Rotational movement of different parts of the larynx were determined with Euler angles.k The rotation of the arytenoid cartilage markers relative to the cricoid cartilage markers was calculated, and the pitch, yaw, and roll rotations about the x-, y-, and z-axes, respectively, were determined. Absolute values for roll, pitch, and yaw were then calculated by subtracting their values at 0 N from that at each force applied; this was performed for all the larynges. The mean maximum roll, pitch, and yaw were then calculated for the 7 larynges at each abduction force applied for the mediolateral and caudocranial suture positions independently.

Statistical analysis

All statistical testing was performed with commercially available software.l The Shapiro-Wilk test was used to assess the distribution of the data. All normally distributed data were expressed as mean ± SD and nonnormally distributed data as median and range.

Mixed-effect models were fitted to the airway biomechanics data (airflow, TP, and TI) with horse included as a random effect. Suture position and the predetermined abduction force applied were included as fixed effects. To determine the difference between the measured changes in airflow biomechanical variables at sequential left-sided arytenoid cartilage abduction forces, Tukey post hoc tests were used. Where appropriate, linear contrast analysis was performed to determine differences in the change of each measure of airway biomechanics (airflow, TP, and TI) across series of measurements obtained at incrementally increased abduction forces. These subsets of measurements were selected for comparison by visual inspection of the mixed-effects model data. Values of P ≤ 0.05 were considered significant.

Results

The amount of force required to elicit maximum left arytenoid cartilage abduction was determined for all the larynges in the study. The median maximum force was 37.86 N (range, 30 to 50 N) when data for both suture positions were combined.

The mean ± SD airflow rates at 0 N of pressure (no left arytenoid cartilage abduction) were 25.57 ± 2.01 L/s for the caudocranial suture position and 28.03 ± 4.81 L/s for the mediolateral suture position. The rates at maximum left arytenoid cartilage abduction were 63.46 ± 5.10 L/s for the caudocranial suture position and 64.33 ± 7.56 L/s for the mediolateral suture position. The mean airflow rate through each larynx increased rapidly from the value at 0 N until 25% of the maximum force was applied; at this amount of force, the mean ± SD LRQ was 0.62 ± 0.25 for caudocranial sutures and 0.67 ± 0.29 for mediolateral sutures. After this point, the rate of increase appeared to slow; a plateau was reached at 50% of maximum force (LRQ, 0.84 ± 0.18 and 0.79 ± 0.24 for caudocranial and mediolateral sutures, respectively). The rate of change in airflow up to 50% of maximum abduction force was significantly (P = 0.001 [linear contrast analysis]) different from the changes produced with incrementally increased forces of 50% to 100% of maximum force for both suture positions. This pattern of increasing airflow corresponded with abduction of the left arytenoid cartilage increasing the lumen size of the rima glottis.

The mean ± SD TP at 0 N abduction force was 227.08 ± 21.51 cm H2O for the caudocranial suture position and 225.94 ± 22.04 cm H2O for the mediolateral suture position, compared with 13.25 ± 7.29 cm H2O and 12.20 ± 5.79 cm H2O for caudocranial and mediolateral sutures, respectively, at maximum force. Evaluation of mean TP data revealed a sharp decrease from the measurement at 0 N when the lowest increment of pressure (8% of the maximum value) was applied (LRQ, 0.40 ± 0.19 for caudocranial sutures and 0.44 ± 0.17 for mediolateral sutures), followed by a more gradual decline with subsequent force increases until 33% of maximum force (LRQ, 0.72 for both suture positions) was reached, at which point a plateau was reached. The rate of change in TP up to 33% of maximum force was significantly (P = 0.001 [linear contrast analysis]) different from the changes produced with incrementally increased forces from 33% to 100% of the maximum force for both suture positions.

The mean ± SD TI decreased from 8.95 ± 1.28 cm H2O/L/s at 0 N to 0.20 ± 0.27 cm H2O/L/s at maximum force for the caudocranial suture position (Figure 3). For the mediolateral suture position, the TI values decreased from 8.31 ± 1.74 cm H2O/L/s at 0 N to 0.23 ± 0.33 cm H2O/L/s at maximum force. A sharp decrease in TI was observed at 8% of the maximum force (LRQ, 0.40 ± 0.19 for caudocranial sutures and 0.44 ± 0.17 for mediolateral sutures), with more gradual decreases between 8% and 42% (LRQ, of 0.80 ± 0.21) of the maximum force for caudocranial sutures and between 8% and 58% (LRQ, 0.80 ± 0.24) for the mediolateral suture, after which there was minimal change for either suture position. The rate of change in TI up to 42% of the maximum force for the caudocranial sutures and 58% of maximum force for the mediolateral sutures was significantly (P = 0.01 for both comparisons [linear contrast analysis]) different from the rate of change produced from 42% to 100% of the maximum force for the caudocranial suture and 58% to 100% of the maximum force for the mediolateral suture. On visual inspection, the caudocranial suture position appeared to have lower TI at lower percentages of maximum abduction force, compared with a mediolateral suture position.

Figure 3—
Figure 3—

Plot of mean ± SD TI and LRQ before left arytenoid cartilage abduction (0 N [0% of maximum abduction force]) and at 12 incrementally increased left arytenoid cartilage abduction forces applied through laryngoplasty sutures up to a previously determined maximum value (the force at which greater tension on the suture did not cause further visible movement of the arytenoid cartilage [100%]) for larynges from 7 equine cadavers in ex vivo experiments. A vacuum with constant suction strength was secured to tubing at the caudal end of the larynx to simulate inspiratory airflow, and 5 measurements/variable were obtained at 10-second intervals for each abduction force applied and each of 2 laryngoplasty suture positions (caudocranial and mediolateral) through the left MPA. For all experiments, the right arytenoid cartilage was secured at maximum abduction with a mediolateral laryngoplasty suture. The change in TI for abduction forces from 8% to 42% of the maximum value was significantly (P = 0.01) different from the change in TI for forces from 42% to 100% of the maximum value in linear contrast analysis for both caudocranial (crosses) and mediolateral (squares) suture positions. There was no discernible difference in LRQs between caudocranial (circles) and mediolateral (triangles) suture positions.

Citation: American Journal of Veterinary Research 81, 8; 10.2460/ajvr.81.8.665

The angle of the right arytenoid cartilage maintained a fairly constant abduction of 37° to 39° for each larynx, with a maximum SD of 6.39° after stabilization by prosthetic laryngoplasty at the maximum abduction force. The angle of the left arytenoid cartilage varied considerably with the percentage of maximum force applied to the suture, up to maximum mean ± SD measurements of 35.16 ± 5.73° for the caudocranial suture position and 34.95 ± 6.19° for the mediolateral suture position.

The mean ± SD CSA of the rima glottis increased sharply up to 25% of maximum force, with a more gradual increase up to 50% of the maximum force for both suture positions (LRQ, 0.84 ± 0.18 with a CSA of 13.25 ± 5.02 cm3 for the caudocranial suture position [92% of maximum area]; LRQ, 0.79 ± 24 with a CSA of 11.95 ± 5.18 cm3 for the mediolateral suture position [77% of maximum area]) and minimal increases thereafter. This corresponded with the airflow measurements, which also did not change significantly between 50% and 100% of the maximum abduction force. The TI continued to decrease marginally up to the maximum abduction force; CSA of the rima glottis (including the vocal folds) at maximum abduction of the left arytenoid cartilage was 14.36 ± 3.75 cm3 for the caudocranial suture position and 15.52 ± 5.15 cm3 for the mediolateral suture position, compared with 11.39 ± 3.23 cm3 for the caudocranial suture position and 12.54 ± 4.02 cm3 for the mediolateral suture when the vocal folds were excluded from this measurement. The vocal folds comprised 20.6 ± 5% of the total CSA of the rima glottis at maximum abduction. Percentage CSA for the rima glottis plotted against percentage force data is provided (Figure 4).

Figure 4—
Figure 4—

Mean ± SD percentage CSA of the rima glottis (quotient of the CSA at each abduction force divided by the maximum CSA of the rima glottis for the same larynx) for the specimens in Figure 3. At most forces ≤ 50% of the maximum value, the CSA of the rima glottis was subjectively greater for a caudocranial suture position than for a mediolateral suture position. See Figure 3 for key.

Citation: American Journal of Veterinary Research 81, 8; 10.2460/ajvr.81.8.665

Assessment of left arytenoid cartilage rotational movement by 3-D biomechanical modeling revealed that, of the 3 movement types, absolute roll had the smallest deviation from the zero coordinates, with the greatest mean ± SD change of −5.03 ± 3.14° for the caudocranial suture position at 50% of maximum force and an arytenoid angle of 31.49 ± 2.83°, whereas that for the mediolateral suture position was −3.47 ± 1.07° at maximum force and an arytenoid angle of 34.95 ± 6.19°. Absolute pitch had the greatest deviation from the zero coordinates; the greatest mean ± SD changes were 53.3 ± 15.9° for caudocranial and 55.41 ± 13.66° for mediolateral sutures, both at maximum force, corresponding to arytenoid angles of 31.49 ± 2.83° and 34.95 ± 6.19°, respectively. On visual inspection, pitch appeared to be slightly improved (ie, slightly greater) with the mediolateral suture placement (Figure 5). The largest deviation in absolute yaw was −34 ± 9° for caudocranial sutures and −44 ± 6.6° for mediolateral sutures, both at maximum force, at arytenoid angles of 35.16 ± 5.7° and 35.16 ± 5.73°, respectively. Pitch and yaw produced a linear pattern graphically after a sharp increase between 0% and 17% of maximum force, with no plateau seen. The continued increase in pitch might have contributed to the continued subtle decrease in TI beyond 50% of maximum abduction force (Figure 6).

Figure 5—
Figure 5—

Plot of mean ± SD pitch (degrees of rotation around the x-axis) and arytenoid angle for the specimens in Figure 3 at the same abduction forces. On visual inspection, pitch was slightly improved (ie, slightly greater) for the mediolateral suture positions (squares), compared with caudocranial suture positions (crosses). Arytenoid angles at each abduction force measurement are shown for caudocranial and mediolateral suture positions (circles and triangles, respectively).

Citation: American Journal of Veterinary Research 81, 8; 10.2460/ajvr.81.8.665

Figure 6—
Figure 6—

Mean ± SD TI (log10-transformed values) for the caudocranial (crosses) and mediolateral (squares) suture positions and pitch for the same suture positions (circles and triangles, respectively) for the specimens in Figure 3 at the same abduction forces. The TI data were log transformed to demonstrate the subtle continued decreases up to 100% of maximum abduction force.

Citation: American Journal of Veterinary Research 81, 8; 10.2460/ajvr.81.8.665

The marker placed at dorsal midline between the arytenoid cartilages had the least displacement around the 3 axes (x, y, and z), compatible with the anatomic location. The ventral corniculate marker had the most movement around the x- and z-axes, whereas markers on the left MPA were displaced the most around the y-axis. There was no discernible difference among the displacements of any of the 3 arytenoid cartilage markers around the y- or z-axes. The displacement of all 3 of these markers was roughly linear around the x-axis. Around the y-axis, all 3 markers were displaced caudomedially.

Discussion

In our ex vivo model, airflow velocities comparable to those for horses at a gallop or maximum exertion were used (63.46 ± 5.10 L/s and 64.33 ± 7.56 L/s, respectively). In vivo inspiratory airflows of 56.3 ± 3.2 L/s and 75.52 ± 9.35 L/s have been recorded at a gallop22 and at maximum exertion (on the basis of maximum heart rate measurements)3 in exercising horses, respectively. Early ex vivo models used much lower airflow velocities of 40 and 42 L/s; therefore, the data from earlier studies23 must be interpreted with caution. The restoration of exercise tolerance in performance animals such as racehorses is the primary rationale for prosthetic laryngoplasty; therefore, a model that provided airflow rates similar to those for horses exercising at maximum intensity was most suitable to evaluate the effects of prosthetic laryngoplasty on airflow dynamics.

Airflow, TP, and TI in equine larynges (with the right arytenoid cartilage fixed in full abduction by routine prosthetic laryngoplasty) altered rapidly from the measurements obtained with no abduction of the left arytenoid cartilage when low forces were applied to suture placed through the MPA in a craniocaudal or mediolateral fashion (up to 25%, 33%, and 8% of maximum abduction force, respectively, with incremental force values creating incremental increases in left arytenoid cartilage abduction). Beyond 50% of the abduction force (LRQ of 0.84 for the caudocranial suture and 0.79 for the mediolateral suture), no significant changes in any of the airway measures were seen, although TI continued to decrease marginally up to the maximum abduction force (100%). We considered the plateau of airflow variables resulted from the smaller diameter of the trachea limiting airflow; in horses, diameter of the trachea is approximately 20% smaller than that of the larynx. Results of a previous study13 revealed that ≥ 25% reductions in CSA of the rima glottis significantly reduce airflow rate, so when abducting the left arytenoid cartilage, the potential limiting effect of tracheal diameter must be considered. In our model, 50% of the maximum abduction force corresponded to 92% of the maximum CSA of the rima glottis for the caudocranial suture position and 77% of the maximum CSA of the rima glottis for the mediolateral suture position, with a left arytenoid angle of approximately 30° and a CSA of approximately 13 cm3 for both suture positions. Although the difference was nonsignificant, CSA of the rima glottis at 50% of the maximum abduction force was numerically greater for caudocranial sutures than for mediolateral sutures. We speculated that this apparent difference was attributable to the slightly greater pitch movement detected for mediolateral sutures. Perkins et al16 demonstrated that pitch results in caudal displacement of the arytenoid facet, which places tension on the arytenoid ligament and causes the arytenoid cartilage to rotate medially into the lumen of the rima glottis, resulting in a smaller CSA. Our findings indicated that a rima glottis CSA of approximately 13 cm3 and left arytenoid angle of 30° would allow an airflow rate of 61 L/s with a TP of 20 cm H2O, comparable to measurements previously reported22 for galloping horses.

The use of 3-D modeling to characterize the movement of the left arytenoid cartilage relative to the cricoid cartilage at various degrees of simulated laryngeal abduction has been previously described.16 The data regarding overall roll, pitch, and yaw of the left arytenoid cartilage in the present study clearly showed that, similar to previous findings,16 the most influential movement following prosthetic laryngoplasty arose from pitch. Interestingly, in the study reported here, 2-D arytenoid angles and pitch did not follow the same pattern graphically; arytenoid angles, LRQs, and CSAs of the rima glottis had minimal further increases at > 50% of maximum abduction force, whereas pitch continued to increase with increasing forces up to the maximum value. We postulated that the continued increase in pitch may have accounted for the continued decrease in TI beyond 50% of maximum abduction force. We considered it possible that continued pitch movement resulted in an increase in laryngeal volume, producing a funneling effect rather than a sharp change in lumen diameter between the abducted arytenoid cartilage and the trachea. This would result in less turbulent airflow through the larynx and a continued reduction in TI, which may correspond to a reduction in inspiratory noise in clinical cases.

When comparing absolute yaw (rotation around the y-axis) with percentage abduction force, a linear relationship was apparent when deviating in a caudomedial direction. This corresponds to movement of the left arytenoid cartilage during tightening of the prosthesis suture; the movement is likely restricted by the cricoarytenoid ligament,24 and this was reflected by greater yaw motion with the mediolateral suture position than with the caudocranial suture position (which antagonizes the cricoarytenoid ligament) on visual examination of the data. This motion affects glottal lumen volume by drawing the arytenoid cartilage dorsally, laterally, and caudally. In combination with the effect of pitch rotating the arytenoid cartilages in a rostral direction, this additionally increases the laryngeal volume and supports that there is an effect on airflow biomechanics in 3 dimensions that cannot be characterized by arytenoid angle and CSA alone. This was reflected in the apparent differences in LRQ, CSA of the rima glottis, and pitch beyond 50% of maximum abduction force in the present study. Although no discernible difference in airflow biomechanics was seen between suture positions, when the 3-D biomechanics of laryngeal abduction are considered, the slightly improved pitch observed with mediolateral suture positioning through the MPA suggested that this orientation may be superior to caudocranial suture positioning.

One limitation of the present study was the use of an air velocity sensor designed to measure wind speed and direction for meteorologic assessments. This type of sensor is designed for measurement of undisturbed air movement, and its use may have resulted in nonlinear and inaccurate airflow readings. The sensor was chosen because it provides highly accurate readings in its intended settings.25 The authors did not perform a calibration of the air velocity sensor specific to its use in the study, which may have impacted the accuracy of the results. A fiberglass tunnel was used to house the sensors, and this was intended to help prevent inaccuracies in airflow data and reduce turbulent airflow. Another important limitation of our study was the failure to remove the vocal folds. On the basis of measurements in this study, the vocal folds accounted for approximately 20% of the total CSA of the rima glottis. With the vocal folds in place, greater abduction force is required to achieve maximum abduction, which may result in increased risk of cartilage failure. Our calculations indicated the possibility that better airflow biomechanics could be achieved following vocal cordectomy. Other investigations23,26 found no significant difference in airflow biomechanics following ventriculocordectomy, despite an increase in CSA. Further ex vivo studies that include removal of the vocal folds may better determine whether this has a significant effect on airflow measures.

We hypothesize that the intrinsic relationship between TI, airflow, and left arytenoid cartilage abduction is responsible for improved outcomes reported12 for horses exercising at less than maximum intensities with lesser degrees of arytenoid cartilage abduction (60% to 80% of maximum). Future studies that include altering the airflow rate through the larynx at various degrees of arytenoid cartilage abduction are required to test this hypothesis.

Acknowledgments

No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there was no conflict of interest.

Presented in abstract form at the 28th Annual Scientific Meeting of the European College of Veterinary Surgeons, Budapest, July 2019.

The authors thank Brian Cox, Royal Veterinary College, for assistance with the figures.

ABBREVIATIONS

CSA

Cross-sectional area

LRQ

Left-to-right angle quotient

MPA

Muscular process of the arytenoid cartilage

TI

Translaryngeal impedance

TP

Translaryngeal pressure

Footnotes

a.

Aerial Specimen Sea, Shakespeare Monofilaments, Columbia, SC.

b.

Ethicon, Johnson & Johnson International, Brussels, Belgium.

c.

Mecmesin Ltd, Horsham, England.

d.

WindSonic Device, Gill Instruments Ltd, Lymington, England.

e.

Digital manometer HHP 201, Omega Engineering Inc, Manchester, England.

f.

Model DC14, Dyson Inc, Chicago, Ill.

g.

Nikon Coolpix 5400, Nikon UK Ltd, Surbiton, England.

h.

Image J, version 1.50, NIH, Bethesda, Md.

i.

GE Lightspeed Universal Medical Systems, Highland Heights, Ohio.

j.

Mimics, version 10.11, Materialise NV, Leuven, Belgium.

k.

Matlab, version 7.5, The MathWorks Inc, Natick, Mass.

l.

JMP, version 13.0. SAS Institute Inc, Cary, NC.

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