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Immediate, short‐, and long‐term changes in tracheal stent diameter, length, and positioning after placement in dogs with tracheal collapse syndrome

Background Intraluminal tracheal stenting is a minimally invasive procedure shown to have variable degrees of success in managing clinical signs associated with tracheal collapse syndrome (CTCS) in dogs. Objectives Identify immediate post‐stent changes in tracheal diameter, determine the extent of stent migration, and stent shortening after stent placement in the immediate‐, short‐, and long‐term periods, and evaluate inter‐observer reliability of radiographic measurements. Animals Fifty client‐owned dogs. Methods Retrospective study in which medical records were reviewed in dogs with CTCS treated with an intraluminal tracheal stent. Data collected included signalment, location, and type of collapse, stent diameter and length, and post‐stent placement radiographic follow‐up times. Radiographs were used to obtain pre‐stent tracheal measurements and post‐stent placement measurements. Results Immediate mean percentage change was 5.14%, 5.49%, and 21.64% for cervical, thoracic inlet, and intra‐thoracic tracheal diameters, respectively. Ultimate mean follow‐up time was 446 days, with mean percentage change of 2.55%, 15.09%, and 8.65% for cervical, thoracic inlet, and intra‐thoracic tracheal diameters, respectively. Initial mean stent length was 26.72% higher than nominal length and ultimate long‐term tracheal mean stent shortening was only 9.90%. No significant stent migration was identified in the immediate, short‐, or long‐term periods. Good inter‐observer agreement of radiographic measurements was found among observers of variable experience level. Conclusions and Clinical Importance Use of an intraluminal tracheal stent for CTCS is associated with minimal stent shortening with no clinically relevant stent migration after fluoroscopic placement. Precise stent sizing and placement techniques likely play important roles in avoiding these reported complications.


| I N TR ODU C TI ON
Canine tracheal collapse syndrome (CTCS) in dogs is a common irreversible, progressive disease of the large airways that predominately occurs in middle-aged small and toy breed dogs. [1][2][3] It encompasses a variety of conditions including tracheomalacia, dorsal membrane weakness, cartilage ring malformation, or some combination of these leading to variable degrees of raspy, honking breathing, coughing, and dyspnea. 4 The initial treatment of choice is conservative medical therapy that often includes weight loss, decreased activity, minimization of environmental factors that cause anxiety and excitement, and a combination of medications such as corticosteroids, anti-tussives, antibiotics, bronchodilators, tranquilizers or sedatives, anti-histamines, or some combination of these. 5,6 In 1 report, 71% of dogs with tracheal collapse responded well to initial medical therapy and management of secondary causes and remained asymptomatic for 12 months. 6 Surgery is recommended when medical therapy options have failed or in acute, unstable cases.
Two commonly performed surgeries for CTCS to restore the narrowed or obstructed lumen include placement of extra-luminal rings (ELR) and intraluminal stents. Most dogs show immediate clinical improvement after either of these surgeries, and complications are associated with both, 7 but stenting has become a more common treatment because fewer perioperative complications may be associated with stenting. 4 Serious complications have been reported after surgical placement of ELR, including laryngeal paralysis. [7][8][9][10] Intraluminal tracheal stenting is a minimally invasive, image-guided treatment option.
Advantages of stents include the ability to be used in any region of the trachea, short surgery and anesthesia times, and noninvasive placement, 2,7,10,11 but complications are not uncommon. Tracheal stenting is a technically demanding procedure and advanced training is recommended to prevent avoidable errors. Acute complications often are associated with improper stent sizing or deployment leading to stent migration or stent misplacement into the carina, mainstem bronchus, or larynx. 4 Some of the most commonly reported complications include inflammatory or bacterial tracheitis (up to 58%), 7,12,13 stent fracture (up to 42%), 7,12-14 stent migration (up to 37%), 7,12,15 and stent shortening (up to 27%). 12, 16 We have experienced some of these complications, but stent migration and shortening are uncommonly encountered compared to rates previously reported. 7,12,15,16 We suspect that different tracheal measuring and stent placement techniques may account for fewer episodes of stent migration and shortening. In addition, these techniques may help properly predict appropriate stent diameter and length at the time of placement, decreasing the risk of stent misplacement within the cricoid or carina regions.
The purposes of our retrospective study were: (1) to identify immediate post-stent changes in tracheal diameters for prediction of stent length during the procedure, (2) to determine the incidence of stent migration and the degree of stent shortening that occurs after stent placement in the immediate-, short-, and long-term periods during the management of these patients by an interventional radiology service, and (3) to evaluate the inter-observer reliability of radiographic measurements among observers with varying levels of experience. We hypothesized that precise stent sizing and appropriate stent placement techniques would minimize the extent of stent migration and stent shortening over time. Data collected included patient signalment and weight, location and type of tracheal collapse, stent diameter and length, and post-stent placement radiographic follow-up times. Types of tracheal collapse were documented as traditional (tracheomalacia, weakened dorsal tracheal membrane or both) or malformation (firm "W"-shaped rather than "C"-shaped tracheal cartilage rings). 4 Radiography, fluoroscopy (both positive-and negative-pressure ventilation images), and endoscopy were used to determine the type of collapse present.

| Stent sizing and placement
Measurements for stent selection were performed as previously described. 4 Briefly, dogs under general anesthesia were placed in right lateral recumbency with the neck flexed to ensure the trachea was as straight as possible. An esophageal marker catheter (5fr Marker Diagnostic Catheter, Infiniti Medical, Menlo Park, California) was placed over a guide wire to span the entire length of the trachea for calibration of measurements accounting for radiographic magnification. The endotracheal (ET) tube was withdrawn until the cuff was at the level of the cricoid cartilage, and the positive-and negative-pressure ventilation device was attached to the ET tube. Positive-pressure ventilation at 20 cm H 2 O was used to achieve maximal tracheal diameter to obtain maximum cervical, thoracic inlet, and intra-thoracic tracheal diameter and length measurements, followed by negative-pressure ventilation at 210 to 215 cm H 2 O to confirm precise location and extent of collapse. In general, a nominal (relaxed) tracheal stent diameter approximately 2-3 mm larger than the maximal tracheal diameter measured was selected. Tracheal stent length subsequently was determined using a sizing chart provided by the stent manufacturer such that the final stent length achieved would span approximately 10 mm caudal to the cricoid cartilage and 10 mm cranial to the carina. As the stent expands, it simultaneously shortens. By oversizing the stent diameter, the stent will remain in place and not completely expand, and therefore be longer. For example, a stent with nominal dimensions of 14 mm 3 58 mm that expands to 10 mm will be 85 mm long. An appropriately sized Vet Stent-Trachea stent was placed under fluoroscopic guidance as previously described. 4 Briefly, the leading (caudal) edge of the stent was positioned approximately 10 mm cranial to the carina and held stationary as the nose cone was advanced down the trachea during deployment. After approximately 1 =3 length deployment, gentle manipulation RASKE ET AL.

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of the stent delivery system back and forth confirmed that the deployed stent had engaged the trachea sufficiently before continuing deployment. During stent deployment, periodic, gentle, forward (caudal) pressure was applied to the entire delivery system to encourage stent expansion before complete deployment. All stents were placed by, or under the guidance of, a single board-certified veterinary surgeon (C. Weisse). Tracheoscopy was performed after stent placement to confirm appropriate stent position and wall contact. Inter-observer reliability comparing measurements was determined for post-stent length; maximum cervical, thoracic inlet, and intra-thoracic diameter; distance from cricoid; distance from carina; length of C7; length of T4; and, length of dorsal cricoid cartilage. Only the measurements by the diplomate of the American College of Veterinary Surgery were used to determine statistical significance comparing initial stent placement measurements to follow-up radiographic measurements for the previously mentioned time categories.

| Statistical analysis
Baseline descriptive statistics are presented as mean and standard deviation (SD) for normally distributed variables whereas non-normally distributed variables are presented as median and range. Ultimate Inter-observer analysis was carried out to assess the agreement between 2 methods of clinical measurement as described previously. 17 The agreement scale was defined as percentage outliers exceeding 2 SDs from the mean. The defined scale of percentage within the limits was defined as follows: 90% as strong, 80% as good, 70% as moderate, 60% moderately weak, and 50% as weak agreement.
Hypothesized mean analyses were carried out by way of a Student's t test if normality of data were achieved. All analyses were deemed significant at P .05 and carried out using SAS 9.3 (SAS version 9.3; SAS Institute Inc., Cary, North Carolina).

| RE S U L TS
Although 67 dogs were identified as having received single tracheal stents during the study period, only 50 met the inclusion criteria. The  Tables 1 and 2. Initial mean stent length was 26.72% higher than nominal length immediately post-stent placement, 15.89% higher than nominal length at short-term follow-up, 13.00% higher than nominal at long-term follow-up and overall 14.55% higher than nominal length at an ultimate mean follow-up of 446 days. Ultimate overall mean tracheal stent shortening was 9.90%, with 9.44% and 9.74% shortening at short-term and long-term follow-up, respectively. A significant difference was observed for stent length between immediate post-stent placement and all-time categories, specifically   The distance (mm) from cricoid cartilage to the cranial aspect of the stent was not significant for any of the pairwise comparisons, nor was the distance from the carina to the caudal aspect of the stent. There was a significant difference for percentage change of intrathoracic diameter between time comparisons for traditional types, specifically for baseline compared to T1-89 (P < .0001), T90-179 (P < .0001), and T180-364 (P 5 .0012), but the percentage change of cervical and thoracic inlet diameter was not significant and no significant differences were identified for malformation types.

| Traditional versus malformation types
The distance from cricoid cartilage to the cranial aspect of the stent was not significant for any of the pairwise comparisons, nor was the distance from the carina to the caudal aspect of the stent for either traditional or malformation types.

| D ISC USSION
To our knowledge, ours is the first report of tracheal stenting investigating the immediate, short-and long-term dimensional changes and positioning of stents in a large group of dogs. Our results suggest that use of an intraluminal tracheal stent for CTCS is associated with minimal, acceptable, and predictable stent shortening with no relevant stent migration after fluoroscopic placement using the measurement and placement guidelines employed by our interventional radiology service.
Using these guidelines, initial stent length was 26.72% higher than nominal length, and ultimate long-term tracheal stent shortening was only 9.90%. Additionally, good inter-observer reliability was found for all measurements between 2 observers of different experience level.
To investigate changes that occurred over time, differences were of clinical signs because of severe collapse cranial to the stent. 16 The stent type and diameter used along with the placement technique may account for these differences.
Complications have been noted with the use of airway stents for the treatment of malignant and benign airway obstruction in human medicine, similar to those seen in dogs, including stent migration, granulation tissue formation around the stent, problems with mucociliary clearance, poor patient tolerance, problems with placement and removal, and stent fracture. [18][19][20] Although complications are similar, the differences between airway collapse in humans and dogs preclude direct comparisons from being made. Advances in stent designs, improvements in stent placement techniques, and understanding and addressing the diversity of CTCS will likely lead to a decrease in these complications.
When appropriately sized diameter stents are used, migration is minimal. Using the maximal cervical and intra-thoracic tracheal diameters is important to anticipate the degree of stent expansion that will occur. 4 No significant differences for mean percentage change in  However, it was noted that there was a high percentage of underestimation of stent length from the prediction techniques used in that study, which ultimately could lead to an inappropriate fit of the stent and increased risk for potential complications. 24 In our study, we found the stent sizing and placement techniques described as critical to limit subsequent stent shortening and migration.
Experience level did not have an effect on tracheal measurements in our study, as good agreement was found between the 2 observers.
Only rare instances of inter-observer differences were identified. The good agreement could be attributed to the systematic way that the measurements were taken in our study. The use of the lengths of the dorsal cricoid cartilage and of the C7 and T4 vertebral bodies appeared to provide an accurate means of measurement to adjust for radiographic magnification in subsequent images that did not have radiographic markers in place. Comparatively, the previously mentioned study evaluating accuracy of segmental measurement techniques found good to high intra-and inter-observer reliability for all segmental measurements among 4 observers of different experience level. 24 Our study had several limitations including its retrospective nature.
Although there was a recommended time for follow-up after stent placement, the number of follow-up examinations and the time between these examinations varied considerably among the dogs.
Future prospective studies with uniform follow-up times are warranted.
Because of the retrospective nature of our study, we could not determine why some dogs were not returned for follow-up at the suggested time intervals. Sample size was small, and fewer than half of the dogs had a follow-up time > 90 days, which may have resulted in a low power of detection for significant differences. Additionally, not all dogs contributed a measurement in each time category and individual dogs accounted for > 1 measurement during some time periods. For example, time period T1-89 had 45 measurements of 37 dogs. Another limitation is that not all follow-up radiographs included the calibration marker. In these cases, calibration of the radiograph depended on either using the length of the vertebral body of C7 or T4 or the dorsal cricoid cartilage that was measured during stent placement. Using these measurements for some cases could have added more variability to the stent diameter and length measurements, because the individual performing the measurements chose which structure (C7, T4, or dorsal cricoid cartilage) was most clearly defined on the radiographs for calibration. This factor also could have led to some variability in measurements. However, based on the good agreement between the observers, we do not believe this factor had an adverse effect. Also, although inter-observer reliability was investigated, repeated measurements performed by the same individual were not investigated to determine the contribution of intra-observer variability.
In conclusion, treatment of CTCS by fluoroscopic placement of intraluminal tracheal stents in dogs resulted in minimal and acceptable mean stent shortening with no evidence of substantial migration in the immediate, short-, or long-term. Inter-observer reliability of radiographic measurements was good. With appropriate sizing and deployment techniques, minor stent shortening appears to occur in the short-term without progression, and migration should be minimal during any time period. Future prospective studies are needed to further assess long-term changes in tracheal stent diameter, length, and position, as well as the clinical relevance of any of these changes for traditional and malformation types of CTCS.

CONFLICT OF INTEREST DECLARATION
Dr. Weisse is a consultant for Infiniti Medical, LLC.

OFF-LABEL ANTIMICROBIAL DECLARATION
Authors declare no off-label use of antimicrobials.

INSTITUTIONAL ANIMAL CARE AND USE COMMITTEE (IACUC) OR OTHER APPROVAL DECLARATION
Authors declare no IACUC or other approval was needed.