Fluoroscopic and radiographic assessment of variations in tracheal height during inspiration and expiration in healthy adult small-breed dogs

Abstract

The objective of this study was to document tidal variations in tracheal height during normal respiration in 19 healthy adult (> 1 y old) small-breed dogs (< 10 kg) using fluoroscopy and radiography. Each dog underwent tracheal fluoroscopic examination on inspiration and expiration while in a standing position (F-S) and in right lateral recumbency (F-RL), followed by radiographic projections obtained in right lateral recumbency. The percent variation in tracheal height during maximal inspiration and expiration was determined at 3 different locations [cervical region (CR), thoracic inlet (TI), and intrathoracic (IT) region]. When all imaging procedures and sites of measurement were considered, tracheal height varied during physiologic inspiration and expiration from 0% to 21.1%, with a mean of 4.5%. The mean percent variation in tracheal height was not significantly different among imaging modalities (F-S versus F-RL versus radiography) (P = 0.16) or measurement sites (CR versus TI versus IT) (P = 0.89). The body condition score (BCS) (P = 0.96), age (P = 0.95), and breed (P = 0.19) did not significantly influence the mean percent variation in tracheal height. The average variation in tracheal height during maximal physiological inspiration and expiration is small (< 6%) in most healthy adult small-breed dogs as assessed by fluoroscopy and radiography, although tracheal height may vary by as much as 21.1% in some healthy individuals. Inspiratory and expiratory radiographs acquired in right lateral recumbency provide an accurate assessment of tracheal height as an alternative to fluoroscopy.

Introduction

Airway collapse is a common contributing factor to chronic cough in dogs, particularly in middle-aged small- and toy-breed dogs (1). This disease is multifactorial and often involves degeneration of the tracheal cartilage rings, which leads to dorsoventral flattening of the trachea and laxity of the dorsal tracheal membrane. Collapse may be focal, regional, or generalized and can affect the cervical region, thoracic inlet or intrathoracic region, large bronchi, or small airways (2). Based on the severity of variations in tracheal luminal diameter assessed by bronchoscopy, the following 4 grades of tracheal collapse have been established: grade 1 — variation in tracheal luminal diameter of 25% to 30%; grade 2 — variation of 30% to 60%; grade 3 — variation of 60% to 90%; and grade 4 — variation of 90% to 100% (3,4).

Given the dynamic nature of the disease and the small size of some affected airways, airway collapse is difficult to definitively diagnose and presents a daily challenge to small animal veterinary practitioners. Clinical signs such as stridor, wheezing, and coughing may guide the clinician toward respiratory disorders affecting the trachea, airways, or pulmonary parenchyma. A wide array of imaging modalities is available to document morphologic changes affecting these structures. These include radiography, fluoroscopy, bronchoscopy, and computed tomography (CT) scan, each of which has specific advantages and limitations.

Radiography has been used extensively to evaluate the trachea and lungs as it is non-invasive, does not require general anesthesia, and most veterinary clinics are equipped with X-ray units. While standard radiography is variably helpful in depicting tracheal collapse, with 60% to over 90% diagnostic success, it tends to underestimate the degree of tracheal collapse (5). As extrathoracic airways are more likely to collapse on inspiration and intrathoracic airways tend to collapse during expiration (2), both inspiratory and expiratory lateral radiographs are often recommended to increase the likelihood of detecting airway collapse. It is also more difficult to diagnose bronchial collapse on radiographs, especially in small-breed dogs.

Fluoroscopy is non-invasive, does not require anesthesia or deep sedation, and can be done in real time while the patient is resting. Carrying out a fluoroscopy after eliciting a cough by tracheal palpation or short bouts of exercise may help identify dynamic disorders (2,6). It is limited to evaluating the trachea and its bifurcation, as well as the principal bronchi in small breeds, however, and provides a poor assessment of small airways and pulmonary parenchymal changes.

Bronchoscopy provides excellent visualization of the luminal aspect of the trachea, principal bronchi, and lobar bronchi, but it does not allow assessment of small airways and pulmonary parenchyma, is invasive and requires general anesthesia, and provides subjective results (2). Despite this, some studies refer to bronchoscopy as the diagnostic test of choice for identifying airway collapse (7,8). According to a recent study, however, fluoroscopy while eliciting coughing is considered more specific than radiography and bronchoscopy for diagnosing tracheal collapse (2).

In recent years, modern computed tomography (CT) units with faster acquisition capabilities have been increasingly used to investigate disorders affecting large and small airways and pulmonary parenchyma. Unlike radiography, fluoroscopy, and tracheobronchoscopy, it provides excellent non-invasive, cross-sectional visualization of airways of various caliber that in turn can be easily measured. While it can be carried out without chemical restraint in patients at risk for anesthesia, motion artefact is best avoided with ventilator-controlled anesthesia.

The tracheal cross-sectional area of healthy dogs can change by up to 24% (mean: 5.5%) from inspiration to expiration (9). However, variations in tracheal dimensions between phases of respiration are often evaluated by inducing positive inspiratory pressure and simulated end expiration. The largest percent variation in tracheal dimensions from inspiration to expiration seems to occur in tracheal height in the cervical region (9).

The main issue with the various diagnostic modalities is that the degree of dynamic variation in tracheal luminal diameter during tidal breathing in clinically normal dogs has not been determined. In clinically normal humans, computed tomography (CT) has revealed that the tracheal diameter can change by 12% to 32% (10) from maximal inspiration to expiration. This range is likely higher than would be expected in dogs because forced inspiration and expiration cannot be easily achieved during radiography or fluoroscopy and there would probably be less variation in tracheal diameter between inspiration and expiration.

Fluoroscopy appears to be the best imaging modality for evaluating tidal variations in tracheal height in dogs, as tracheal height can be evaluated dynamically, without any influence of sedation or anesthesia. Moreover, it has not been described in the literature whether fluoroscopic examinations in a standing position allow better visualization of bronchial collapse and whether the measurements are similar between F-S and F-RL, which are frequently carried out in practice.

The objective of this study was to document tidal variations in tracheal height in adult small-breed dogs with no clinical signs or recent history of respiratory disease, using fluoroscopy [standing fluoroscopy (F-S) and right lateral recumbency fluoroscopy (F-RL)] and inspiratory and expiratory radiographs (right lateral recumbency). First, we wanted to specifically determine the percent variations in tracheal height during inspiration and expiration at 3 sites of measurement [cervical region (CR), thoracic inlet (TI), and intrathoracic (IT) region]. Second, we evaluated whether these variations differed significantly depending on the type of examination or site of measurement and third, whether the tracheal height measurements (mm) were significantly different between the 2 types of fluoroscopic positioning (F-S or F-RL) at each site of measurement. Fourth, the influence of body condition score (BCS), age, or breed on the tidal variations of tracheal height was assessed. Finally, we wanted to estimate whether the magnification induced in our imaging procedures (fluoroscopy and radiography) was significantly different in the 2 types of radio-opaque markers used, i.e., catheter and ruler.

We hypothesized that variation in tracheal height from inspiration to expiration, as evaluated by fluoroscopy and radiography, would not exceed 24% (9). Moreover, we speculated that neither the fluoroscopic position (F-S, F-RL) during acquisition nor the site of measurement (CR, TI, IT) would impact variation in tracheal height from inspiration to expiration and from fluoroscopy to radiography (right lateral recumbency, images taken at inspiration and expiration).

We expected that the percent variation in tracheal height would be influenced by the body condition score (≤ 5/9 or > 5/9), age (≤ 6 y old or > 6 y old), and breed of the dogs in our study, depending on the type of imaging procedure and/or the site of measurement. More precisely, we hypothesized that the percent variation in tracheal height would be significantly greater in older dogs (> 6 y old), as tracheal collapse is a progressive disease, dogs with a body condition score of > 5/9, as obesity is a well-known risk factor for tracheal collapse (1), or dogs belonging to a breed at risk.

Materials and methods

Patient selection

The study was conducted at the Faculty of Veterinary Medicine of the University of Montreal from November 1, 2016 to May 30, 2017. This study was approved and conducted in accordance with the Committee for the Ethical Use of Animals of the Faculty of Veterinary Medicine, University of Montreal.

Dogs recruited to participate in the study belonged to students, staff, and clients from the general practice. Dogs were enrolled if they were > 1 y old, weighed < 10 kg, and had no recent history (< 1 mo) of respiratory disease and no respiratory signs, e.g., coughing, excessive panting or reverse sneezing, sneezing, and intolerance to exercise.

A 10-kg cutoff weight was determined in order to recruit adult dogs belonging to breeds at risk of tracheal collapse. Dogs were excluded from the study if respiratory anomalies were detected during physical examination, if they were too agitated to allow examination without chemical restraint, or if a thoracic lesion (mediastinal, pleural, alveolar, structured interstitial, or heavy unstructured interstitial) was observed on radiographic projections.

Owners provided written consent before enrolling in the study. A thorough physical examination was carried out before imaging. On the day of imaging, owners were asked about their dog’s medical history, vaccination status, and current therapy.

Imaging protocol

Fluoroscopic and radiographic images were acquired with a high frequency Siemens AXIOM Iconos R200 (Siemens, Mississauga, Ontario). A cineloop encompassing 3 respiratory cycles was first recorded with a horizontal beam while the dog was standing (F-S) and then with a vertical beam after placing the dog in right lateral recumbency (F-RL) (Figure 1). Each cineloop was reviewed to ensure that the caudal aspect of the larynx and the entire diaphragm was included during all 3 respiratory cycles.

Figure 1.

Tracheal height assessment was performed on images obtained during fluoroscopic and radiographic acquisitions in right lateral recumbency (A, B) and in a standing position (C, D). A — Right lateral recumbent images were obtained with a vertical X-ray beam. B — Close-up image of A illustrating placement of the radio-opaque catheter marker (*) along the sternum using a small clip (black clip on the dog’s hair). The radio-opaque ruler (black arrow) was secured on the table using tape immediately ventral to the dog’s sternum. C — The X-ray beam was rotated horizontally to obtain left to right lateral projection of the thorax in a standing position. D — Close-up image of C illustrating placement of the radio-opaque catheter marker (*) disposed along the dorsal spinous processes of the vertebral column, whereas the radio-opaque ruler is secured directly on the examination table ventral to the dog’s head and neck.

Digital radiographic (DR) projections using a vertical beam were then acquired in inspiration and expiration while in right lateral recumbency, followed by ventrodorsal and left lateral recumbent projections taken in inspiration. A marker catheter (Infiniti Medical, Redwood City, California, USA) was fixed with small clips along the spinous processes or the sternum to provide a calibration tool for measuring tracheal height A radio-opaque ruler was also placed directly on the table along the sternum of each dog and for each imaging procedure, in order to compare the magnification induced by the imaging procedures of the 2 radio-opaque markers (Figure 1A–D) The focal detector distance was kept constant throughout the study.

No chemical restraint was administered for any of the imaging examinations. A research project number attributed through the hospital identification system (HIS) was used as the patient identification number for all dogs, thereby preserving anonymity. Each acquisition was identified with a unique 6-digit requisition number obtained by a number generator, providing a total of 6 different acquisitions for each dog. This information was kept by the radiology technologist and was revealed only after all measurements were completed. Fluoroscopic and radiographic images were transferred to a picture archiving and communication system (PACS) and reviewed using the digital radiography imaging system AGFA Impax 6 (Agfa, Toronto, Ontario). All measurements were taken over a period of 1 mo after the study was completed, in a blind randomized manner, and reviewed by a Board-certified veterinary radiologist (DACVR).

Fluoroscopic assessment and measurements

Each cineloop was reviewed using a frame-by-frame mode allowing selection of each frame demonstrating maximal inspiration and expiration, respectively, based on movements of the diaphragm, during 3 respiratory cycles for a total of 6 frames selected per acquisition. Selected frames from one respiratory cycle performed during fluoroscopic examination are shown in Figure 2 (A–D). Those frames show the movement of the diaphragm during spontaneous breathing, allowing definition of maximal inspiration and expiration. Maximal inspiration was defined as the maximal caudal excursion of the diaphragm (Figure 2A). Maximal expiration was defined as the maximal cranial excursion of the diaphragm (Figure 2C). For each of the 6 selected frames, tracheal height, defined as the distance in millimeters between the dorsal and the ventral borders of the tracheal lumen, was measured at the following 3 locations: the level of the C4–C5 intervertebral disc space (CR); C7–T1 (TI); and T3–T4 (IT), as illustrated in Figure 3 (A–B). Three measurements of tracheal height at maximal inspiration and 3 measurements at maximal expiration were determined successively at each site and then averaged.

Figure 2.

Selection of fluoroscopic images for maximal inspiration and expiration based on excursion of the diaphragm in a healthy small breed dog. A–D — Selected frames from one respiratory cycle performed during fluoroscopic examination showing the movement of the diaphragm during spontaneous breathing. A — Maximal caudal excursion of the left crus of the diaphragm (large arrow) during one respiratory cycle reaching the landmark 2 was designated as maximal inspiration. B — Intermediate excursion of the left crus of the diaphragm (large arrow) corresponding to the half-way location between landmark 1 and 2. C — Maximal cranial excursion of the left crus of the diaphragm (large arrow) during one respiratory cycle reaching the landmark 1 was designated as maximal expiration. D — After expiration, the left crus of the diaphragm moves caudally, reaching an intermediate position between landmark 1 and 2 as seen on image B. * — indicates location of the larynx; T9 — 9th thoracic vertebra.

Figure 3.

Measurement sites of tracheal height at maximal inspiration (A) and expiration (B). First, lines (white lines) were traced at the level of C4–C5 (1), C7–T1 (2) and T3–T4 (3) intervertebral disc spaces. Using these lines as guides, tracheal height was then measured for the cervical (CR), thoracic inlet (TI), and intra-thoracic (IT) regions by tracing a line (black lines) perpendicular to the dorsal and ventral luminal borders of the trachea as close as possible to the guideline. The diaphragm (arrow) and caudal end of the larynx (*) were included on each image. The distance between two marks on the catheter marker (d1) and the ruler (d2) was measured on each image [for image clarity purposes, these distances are only illustrated on the top image (A)]. Each calibration device is identified on the bottom image (B). T10, represents the vertebral body of the 10th thoracic vertebra.

Radiographic assessment and measurements

Digital radiography (DR) projections were used to assess each dog’s airways and pulmonary parenchyma on the day of acquisition and to identify a redundant dorsal tracheal membrane when present. Only right lateral recumbent DR projections were used for measurements. Tracheal height was measured at the same 3 locations described for the fluoroscopic images on both inspiratory and expiratory DR projections (Figure 3A–B).

Measurements using the marker catheter and the radio-opaque ruler

Tracheal height measurements were adjusted, taking into account the magnification induced by the imaging procedures, by first measuring the distance between 2 radio-opaque marks on the marker catheter, which should correspond to 10 mm. The tracheal height measured in absolute value (mm) was then adjusted according to the magnification obtained. For example, on most images, the distance between the 2 marks was equivalent to 11 mm, corresponding to a magnification of 10% (Figure 3A–B), which was then subtracted from the measured tracheal height in millimeters to account for magnification, e.g., a measured tracheal height of 11 mm and a magnification of 10% = adjusted tracheal height of 10 mm.

Measurements were also taken between 2 marks on the ruler, which was placed directly on the table, in order to identify if there was a significant difference in terms of magnification between the ruler, which is more convenient to use as it is placed directly on the table, and the marker catheter.

The mean tracheal height for each location, position, and respiratory phase was used to determine the percent tracheal height variation during maximal inspiration (maxinsp) and expiration (maxexp), according to the modality used, using the following equation:

$$\%\hspace{0.17em}Tracheal\hspace{0.17em}height=\frac{(mean\hspace{0.17em}tracheal\hspace{0.17em}height\hspace{0.17em}at\hspace{0.17em}maxinsp-mean\hspace{0.17em}tracheal\hspace{0.17em}height\hspace{0.17em}at\hspace{0.17em}maxexp)}{highest\hspace{0.17em}mean\hspace{0.17em}between\hspace{0.17em}maxinsp\hspace{0.17em}and\hspace{0.17em}maxexp}\times 100$$

Statistical analysis

Fluoroscopic measurements were analyzed using a mixed-linear model with position (F-S versus F-RL) and measurement site (CR, TI, IT) as within-subject factors, including the interaction between the 2 factors. In a further elaboration of this model, potential risk factors were added as additional fixed factors, including body condition score, age, or breed. A paired t-test was used to compare tracheal heights between the 2 fluoroscopic acquisitions (F-S, F-RL).

A similar model was used to analyze the radiographic results and to compare them with those obtained with the 2 fluoroscopic positions.

Results

Twenty-three dogs were recruited for the study, but 4 were excluded because of excessive agitation or anxiety during the imaging procedures. Of the 19 dogs included in the study, 13 were females and 6 were males. The median age was 6 y 4 mo (1 to 15 y) and the median weight was 5.4 kg (1.7 to 9.1 kg). Two dogs had a body condition score (BCS) of 4/9, 12 dogs had a BCS of 5/9, and 5 dogs had a BCS of 6/9. Eleven breeds were represented, including Yorkshire terrier (n = 3), Chihuahua (n = 3), Dachshund (n = 3), Cavalier King Charles spaniel (n = 2), Jack Russell terrier (n = 2), and 1 each of poodle, schnauzer, beagle, shih tzu, cocker spaniel, and Maltese.

Two dogs presented occasional coughing and 4 dogs occasional reverse sneezing at home. These dogs were not excluded from the study since the clinical signs were occasional and had not been observed in the month before the study. All but 1 dog received routine vaccinations, whereas only 11 dogs were vaccinated against Bordetella bronchiseptica. Three dogs had a left apical heart murmur (grade 2/6) during physical examination and 8 dogs coughed on palpation of the trachea. The clinical signs and results of physical examinations for all dogs are presented in Table I. A prolapse of the dorsal tracheal membrane was diagnosed in 6 dogs. This anomaly was either diagnosed on fluoroscopy (2/6), radiography (6/6), or both (2/6). Only half of these 6 dogs coughed on tracheal palpation. Eight dogs had a mild bronchial pattern exclusively noted on thoracic radiographs, which was considered age-related.

Table I.

Clinical signs and physical examination findings of dogs studied.

	Number of dogs (19)	Percentage (%)
Anamnesis
Reverse sneezing	4	21
Vaccination status	18	95
Deworming prevention	14	74
NSAID when neededa	2	11
Physical examination
Body condition score	5	26
Triggerable cough	8	42
Heart murmur	3	16

^aNSAID (non-steroidal anti-inflammatory drug) was administered for disc herniation in 1 dog and for coxo-femoral dysplasia in another dog when the owner felt it was necessary.

Measurements of tracheal height

Tracheal height measurements at all 3 sites (CR, TI, and IT) for both fluoroscopic and radiographic examinations are shown in Table II. In our study, all types of examinations considered (F-S, F-RL, radiography), tracheal height measurements were greater at inspiration than at expiration at TI and IT (67% and 70%, respectively), which supports dynamic narrowing of the intrathoracic airways during expiration. Measurements of the cervical tracheal height were significantly greater on F-RL than those measured on F-S, at both inspiration (P = 0.01) and expiration (P = 0.015). No statistically significant difference was found for tracheal height measurements at other sites between F-RL and F-S or between phases of respiration.

Table II.

Range and mean of tracheal height measurements obtained from fluoroscopic and radiographic examinations according to the dog’s position during the imaging procedure, site of measurement, and phase of respiration (inspiration versus expiration).

Site of measurement	Fluoroscopy		Digital radiography
	Standing Position (mm)	Right lateral recumbency (mm)	Right lateral recumbency (mm)
CR
Inspiration	5.0 to 14.0 (9.1)a	4.8 to 13.4 (10.1)a	6.9 to 14.2 (11.0)
Expiration	4.8 to 12.4 (9.2)a	5.5 to 13.6 (10.0)a	6.9 to 14.1 (10.8)
TI
Inspiration	4.0 to 11.7 (7.9)	3.8 to 11.2 (7.8)	4.5 to 12.0 (8.8)
Expiration	4.0 to 11.1 (7.8)	3.8 to 10.5 (7.6)	4.5 to 11.6 (8.5)
IT
Inspiration	4.2 to 12.5 (8.1)	4.4 to 12.5 (8.3)	5.5 to 13.1 (9.6)
Expiration	4.0 to 11.7 (7.9)	3.8 to 12.1 (8.1)	5.4 to 13.1 (9.3)

In each column, the range of tracheal height measurements is first displayed followed by the mean in between parentheses.

^aP < 0.05.

Percent variation in tracheal height during maximal inspiration and expiration

The percent variation in tracheal height at CR, TI, and IT during maximal inspiration and expiration and for both fluoroscopic and radiographic examinations are given in Table III. The mean percent change of tracheal height variation between maximal inspiration and expiration during fluoroscopic examinations was not higher than 4.7% during F-S and 4% for F-RL (Table III). In F-S, the maximal percent variation was obtained at TI, reaching 21%, whereas IT was associated with the maximal percent change in tracheal height variation during F-RL with a value of 13.5% (Table III).

Table III.

Percent variation in tracheal height during maximal inspiration and expiration according to the dog’s position during fluoroscopic and digital radiography acquisitions and to site of measurement

Type of examination	Range of variation in tracheal height (%)	Mean (%)	Median (%)
Sternal fluoroscopy
Cervical region	0 to 11.9	4.1	3
Thoracic inlet region	0 to 21.1	4.7	3.5
Intrathoracic region	0 to 10.5	4.5	3.4
Right lateral recumbency fluoroscopy
Cervical region	0 to 9.5	4	3.9
Thoracic inlet region	0 to 8.7	3.7	4.2
Intrathoracic region	0 to 13.5	3.6	3.3
Right lateral recumbency digital radiography
Cervical region	0 to 13.3	5.1	4.9
Thoracic inlet region	0 to 10.3	4.6	4
Intrathoracic region	0.8 to 16.4	5.8	4.9

Position during acquisition (F-S versus F-RL) did not significantly impact (P = 0.41) the mean percent of tracheal height variation or did the 3 sites of measurements (P = 0.98). No significant interaction was found between these 2 factors (position during acquisition and sites of measurement) (P = 0.82).

The mean percent change of tracheal height variation between maximal inspiration and expiration during radiographic examinations was not higher than 5.2% (Table III). The maximal percent variation on radiographic examinations was obtained at IT, reaching 16.4% (Table III). The mean percent of tracheal height variation was not affected by the site of measurement along the trachea (P = 0.89) for all imaging procedures or by the imaging modality or position (F-S versus F-RL versus radiography) (P = 0.16). No significant interaction was found between the 2 factors (position during acquisition and sites of measurement) (P = 0.85).

Several subjects (n = 8 dogs) did not demonstrate variation of their tracheal height during maximal inspiration and expiration at certain sites, which explains the zero percent variation of tracheal height frequently obtained, either on fluoroscopic or radiographic examinations. This was more frequently observed at TI and at IT (n = 6 dogs each) for the fluoroscopic examinations and at CR for the radiographic projections (n = 3).

Influence of BCS, age, and breed

The mean percentage of variation in tracheal height was not associated with BCS (P = 0.96), age (P = 0.95), or breed (P = 0.19), regardless of the modality (F-S, F-RL, right lateral recumbency DR) or sites of measurement (CR, TI, IT).

Magnification (marker catheter versus ruler)

For F-RL and right lateral recumbent radiographs (at inspiration and expiration), the magnification induced was significantly greater with the marker catheter than with the ruler (P = 0.032). There was no significant difference, however, in terms of magnification between the marker catheter and the ruler during F-S (P = 0.13). Absolute tracheal height values measured on images were therefore adjusted considering the magnification calculated on the catheter marker, which was believed to more accurately reflect tracheal measurements since the marker was placed at the same height as and parallel to the trachea (Figure 1).

Discussion

This study evaluated variations in tracheal height during inspiration and expiration in adult small-breed dogs with no clinical signs or recent history of respiratory disease, using fluoroscopy (F-S and F-RL) and radiography (right lateral recumbency). The population included 19 dogs of various small breeds: 8 dogs were from breeds considered at risk of tracheal collapse (Yorkshire terrier, Maltese, poodle, Chihuahua, shih tzu) (1); and 11 dogs belonged to breeds with no particular known risk for tracheal anomalies. We chose this healthy small-breed dog population specifically as they are most often presented for evaluation of airway collapse by fluoroscopy and radiography. The goal of this study was to provide a better understanding of the normal variation in tracheal height found in healthy small-breed dogs, in order to help differentiate between airway collapse and normal variations in tracheal diameter in dogs presented for evaluation of airway collapse.

Four dogs were excluded from our study, as it was not possible to carry out fluoroscopy in 3 complete respiratory cycles and radiography without significant restraint and sedation. Since patients presented for suspicion of tracheal collapse are often evaluated without the use of any chemical restraint, including sedation and anesthetics, and our desire was to design a study for which results could be extrapolated to routine evaluation of tracheal height done in the clinic, the use of sedatives was avoided (11,12). We also wanted to limit any possible effect of sedatives or anesthetics on tidal volume and diaphragmatic movement, as has been described in previous studies (11,12).

In accordance with our hypothesis, the percent of variation in tracheal height obtained in our study (0% to 21.1%, mean of 4.5%) was slightly lower than that reported in a previous study of dogs that underwent general anesthesia and evaluation of tracheal height by CT (9). Our results may be explained by the fact that we measured tracheal height during spontaneous tidal breathing using fluoroscopy and radiography, observing movements of the trachea in real time when the patient is at rest and not influenced by sedation or mechanical ventilation forces, which therefore more closely reproduces daily tracheal examination in dogs suspected of having tracheal collapse. In healthy dogs, normal voluntary inspiration creates negative intrathoracic pressure. The intratracheal pressure is therefore negative rather than positive in spontaneously breathing dogs during inspiration. It is reasonable to think that applying positive intratracheal airway pressure during inspiration in an anesthetized animal will affect the tracheal measurements compared to those obtained in spontaneously breathing dogs (9,13).

Despite the relatively low mean percent of variation in tracheal height during inspiration and expiration in our study (4.5%), some individuals (n = 4) presented greater variation (21.1%, 16.4%, 13.5%, 13.3%). Only 4 dogs had variations in tracheal height greater than 10%. The dog with the highest value (21.1% at TI, F-S) was an 11-year-old Maltese with a prolapse of the dorsal tracheal membrane identified on thoracic radiographs. The dog with the second highest values was a 15-year-old cocker spaniel with a percent variation in tracheal height of 16.4% (IT, right lateral recumbency radiography). This individual coughed on tracheal palpation during the physical examination and had a mild diffuse bronchial pattern on thoracic radiographs. It is possible that these 2 dogs had a subclinical tracheal collapse, with no clinical signs or recent history of respiratory disease. These higher variations in height were noted on only 1 imaging procedure for each dog, which makes them even more difficult to interpret. It may also point to the fact that variation in tracheal height during spontaneous breathing is a dynamic phenomenon that may occasionally manifest different patterns. It would be interesting to demonstrate whether intermittent dynamic tracheal collapse is underestimated during a single static evaluation on either fluoroscopy or radiography compared to various other positions and modalities.

Our results demonstrate that radiographs taken in right lateral recumbency offer a good alternative to fluoroscopy for evaluating variations in tracheal height during inspiration and expiration in healthy adult small-breed dogs as no significant difference was found between modalities and/or positions during acquisition (F-S versus F-RL versus radiography). Inspiratory and expiratory radiographs carried out in right lateral recumbency may aid recognition of normal variations in tracheal height in adult small-breed dogs for practitioners without access to fluoroscopy. Since dogs included in our study were healthy and with no clinical evidence of tracheal collapse, we were not able to compare the suitability of radiography with fluoroscopy for diagnosing tracheal collapse in affected dogs, as has been evaluated in previous studies (2,5).

The greater cervical tracheal height measurements in right lateral recumbency fluoroscopy (F-RL) compared to standing fluoroscopy (F-S), at both inspiration and expiration, was not expected. This implies that measurements taken standing and in right lateral recumbency are not identical for the cervical region, which needs to be taken into account when conducting longitudinal studies on an individual. This result could suggest that F-RL should be used if a more accurate measurement of cervical tracheal diameter is required, i.e., in a patient needing a tracheal stent, as the measurements of cervical tracheal height were greater in our study in F-RL than in F-S.

It is sometimes tempting for general practitioners to diagnose a tracheal collapse or redundant dorsal tracheal membrane based solely on history and physical examination, especially if cough is elicited on tracheal palpation. In our study, a redundant dorsal tracheal membrane was visible in 6 dogs on thoracic radiographs and/or fluoroscopy. As cough was elicited on tracheal palpation in only 3 of these dogs, it seems inappropriate to diagnose a tracheal collapse or a redundant dorsal tracheal membrane based only on eliciting cough on tracheal palpation during physical examination. Imaging assessment of the trachea is essential to diagnose airway collapse.

Our study had several limitations. First, its statistical power is relatively low (19 dogs) and a significant difference of mean percent variation in tracheal height may have been identified in a larger sample of dogs. Specifically, 52 dogs would have been necessary to identify a significant difference in mean percent variation in tracheal height between fluoroscopy in right lateral recumbency (F-RL) and right lateral recumbent radiographs, 80% of the time. Hundreds of dogs would have been necessary to identify a significant difference in mean percent variation in tracheal height, 80% of the time, between the other types of imaging procedures or sites of measurement.

Moreover, variations in tracheal height were not related to BCS, age, or breed, as would have been expected. This may also be due to the small sample size of our study. As variations in tracheal height tended to be greater in breeds at risk of tracheal collapse, it is possible that a significant difference between dogs belonging to a breed at risk or not would have been identified with a larger sample size. As tracheal collapse is a slowly progressive degenerative disorder of the tracheal and bronchial cartilaginous rings, it is reasonable to think that tracheal height would vary more in older dogs than in younger dogs (1).

Approximately 25% of dogs included in this study had a BCS of > 5/9. Although obesity is a well-known risk factor for tracheal collapse (1), none of these dogs demonstrated a significantly increased variability in tracheal height during inspiration and expiration, which suggests that other factors may also play a role in manifesting tracheal collapse in overweight dogs. Only 2 of these dogs were breeds considered at risk of tracheal collapse (1 Yorkshire terrier and 1 poodle), however, which makes the comparison of overweight dogs to dogs that are not overweight unsuitable in our study. It would have been interesting to know whether being overweight would increase the variability in tracheal height in a population of dogs all belonging to breeds at risk of tracheal collapse compared to dogs with an optimal BCS.

The results concerning magnification were not conclusive in our study. Our conflicting results could be explained by the greater mobility of the marker catheter placed along the spinous processes or sternum of each animal, from 1 imaging procedure to the other. Even if the marker catheter is a less convenient tool than the table ruler, it is advantageous in order to obtain the most accurate measurements of tracheal height, as it is placed parallel to the trachea and at the same height, which allows the veterinarian to obtain the most accurate measurements of tracheal height despite the magnification induced by the imaging procedure.

The main objective of this study was to document variations in tracheal height at inspiration and expiration in healthy adult small-breed dogs with no clinical signs or recent history of respiratory disease using fluoroscopy in a standing position and in right lateral recumbency (F-S and F-RL) and radiography in right lateral recumbency. Despite its limitations, this study improves our understanding of the degree of fluctuations in tracheal diameter during spontaneous breathing in clinically normal dogs. The assessment of tracheal height in healthy small-breed dogs appears to be similar in fluoroscopy and radiography, allowing general practitioners without access to fluoroscopy to estimate the tracheal height in small-breed dogs using radiography. When diagnosing tracheal collapse, given its dynamic nature, it may be beneficial to use a combination of various imaging modalities.