Introduction
The pharynx and larynx are major components of the upper respiratory system. The pharynx includes the oropharynx, nasopharynx, and laryngopharynx. The oropharynx is separated from the nasopharynx by the soft palate. Finally, the epiglottis separates the oropharynx and laryngopharynx and extends until it just overlaps the tip of the soft palate.1,2 The upper airway is a complex structure that is required to perform the following functions: swallowing, vocalization, and respiration.3 During respiration, the upper airway maintains patency. The upper airway patency is determined by mechanical and neuromuscular factors. The mechanical factor is based on the Starling resistor model and involves the difference in pressure between inspiration and expiration. The neuromuscular factor involves the movement of the pharyngeal dilator muscles, including the sternohyoid, geniohyoid, and genioglossus muscles, that are innervated by the hypoglossal nerve.4,5
Upper respiratory tract diseases are relatively common in veterinary species and can include nasopharyngeal stenosis, dynamic pharyngeal collapse, elongated soft palate, and soft palate edema.5,6,7 These diseases are diagnosed on the basis of findings of several investigative methods, including endoscopy, CT, radiography, and fluoroscopy. Radiography and fluoroscopy are noninvasive diagnostic techniques that can be performed without patients undergoing anesthesia. Furthermore, fluoroscopy is a real-time imaging modality that can detect dynamic changes in the upper respiratory tract during the respiratory cycle. During radiographic or fluoroscopic examination for the evaluation of upper respiratory tract diseases, veterinary patients are positioned in lateral or sternal recumbency or remain in a standing position5,8; if they are awake or mildly sedated, patients are manually restrained or confined (perhaps in a plastic box) to limit their movement. During evaluation of the upper respiratory tract, appropriate patient positioning is important. A mildly extended head posture has been considered to be the most useful position for lateral views. If the patient is oriented with the head in an oblique position, the luminal diameter of the pharynx is underestimated and the sizes of surrounding soft tissue structures, including the soft palate and laryngeal cartilages, are overestimated.9 As a result of poor assessment technique, structures can be mistaken for masses, and suboptimal positioning can make it difficult to diagnose upper respiratory tract diseases.9
In human and veterinary medicine, it is a well-known fact that head posture has an influence on the upper respiratory tract. The Pcrit refers to the pressure at which pharyngeal airflow is occluded and is primarily used as an index for pharyngeal collapsibility.10 In previous studies of humans4 and dogs,11
it was found that the Pcrit increases and decreases when the atlanto-occipital joint is manipulated and the head is flexed and extended, respectively. The results of imaging evaluations of the pharyngeal luminal diameter in relation to head posture indicate that the pharyngeal luminal diameter increases with an extended head posture, compared with the diameter with a neutral head posture, in humans and horses.12,13 When the head is extended, the airway is more resistant to collapse, thereby allowing more airflow into the upper airway. In contrast, flexing the head makes the airway prone to collapse and restricts airflow to the lower airway. However, despite the fact that suboptimal positioning affects the ability to diagnose upper respiratory tract conditions, no studies involving imaging examinations to determine the extent of the influence of head posture on the upper respiratory tract in dogs have been conducted, to our knowledge.
The purpose of the study reported here was to develop a new method for objectively interpreting the effects of head posture during fluoroscopy in dogs. In addition, the effects of flexed and extended head postures on the laryngopharyngeal anatomic structures including the nasopharynx, soft palate, and epiglottis were evaluated. The intent was to determine whether head posture affected the diagnostic criteria and measurements used to assess diseases affecting the laryngopharyngeal anatomic structures. Finally, the effect of sedation on the laryngopharyngeal anatomic structures was evaluated. We hypothesized that head posture would affect the laryngopharyngeal structures, and that the pharyngeal luminal diameter in dogs would vary significantly in relation to head posture as previously described for humans and horses.12,13 In addition, we hypothesized that head posture–induced changes in laryngopharyngeal structures would affect quantitative measurements used as diagnostic criteria for upper respiratory tract disease in dogs.
Materials and Methods
Animals
Six clinically normal Beagles were included in the study. All dogs were sexually intact males with a mean age of 6.2 years (range, 5.8 to 6.5 years), mean weight of 10.4 kg (range, 9.3 to 11.7 kg), and mean BCS of 4.5 (range, 4/9 to 5/9). Each dog was considered healthy and had no evidence of respiratory tract disease on the basis of results of a physical examination, CBC, serum biochemical profile, and thoracic auscultation, radiography, and fluoroscopy. The study was approved by the Institutional Animal Care and Use Committee of Konkuk University (approval No. KU 19104).
Head posture and fluoroscopic examination procedure
For each dog, 3 head postures were established by manipulating the atlanto-occipital joint to alter the position of the head in relation to the neck. When the angle between the imaginary line drawn parallel to the ridge of the nose and the line drawn parallel to the dorsal ridge of the neck measured with a protractor was 90°, 125°, or 160°, the associated head postures were defined as flexed, neutral, and extended, respectively (Figure 1). All dogs were positioned in right lateral recumbency, and fluoroscopic examinationsa of the laryngopharyngeal structures, including the nasopharynx, soft palate, and epiglottis, were performed. For each dog, the order of evaluation of the flexed, neutral, and extended head postures was randomized.b A relaxation interval of ≥ 1 minute was allowed to elapse between each head posture positioning. To prevent head rotation, the muzzle of each dog was manually restrained and positioned so that the dog's tympanic bullae and mandibles overlapped on the fluoroscopic image.14 At least 3 regular respiratory cycles were observed at each head posture, where 1 respiratory cycle was defined as the interval between the beginning of one inspiration to just before the beginning of the next inspiration. Fluoroscopy videos were recorded at a frame rate of 30 frames/s. To investigate the effects of sedation and head posture on the laryngopharyngeal structures, fluoroscopic examination of the laryngopharyngeal structures was first performed with each dog manually restrained with a neutral head posture without sedation. Each dog was subsequently mildly sedated (medetomidine,c 0.015 mg/kg, IM), and fluoroscopic examination of the laryngopharyngeal structures was performed with its head in a neutral head posture.
Fluoroscopic image evaluation
Measurements of interest were obtained from fluoroscopic images in a standardized manner. The ABN was defined as the angle between a line parallel to the ventral border of the basisphenoid bone and a line parallel to the dorsal border of the nasopharyngeal lumen (Figure 2). The TSP was measured perpendicular to the midline at a point that was 1 cm cranial to the tip of the soft palate. The DNL was measured perpendicular to the midline of the nasopharyngeal lumen at the same point where the TSP was measured. The OLES was defined as the length between the tip of the epiglottis and the point at which the epiglottis overlapped the tip of the soft palate. The DET was defined as the shortest distance between the tip of the epiglottis and the tympanic bulla. The maximal and minimal TSP, DNL, OLES, and DET values were measured within 1 respiratory cycle. The PDNLD was determined on the basis of the percentage change in the DNL during a respiratory cycle. The fluoroscopic images were evaluated with image softwared and a postprocessing software application.e Three respiratory cycles were randomly selected from the recorded videos, and all variables were measured 3 times (once during each respiratory cycle) by 1 investigator (YH) who had diagnostic imaging expertise.
Statistical analysis
All the statistical data analyses were performed with a commercial statistical software package.f To assess reproducibility, all the variables were measured 3 times by 1 investigator (YH), and the intra-observer reliability was assessed with an ICC test. For each variable, the mean value was calculated from the 3 respiratory cycles for each dog, and then the median was calculated for all 6 dogs. The effects of sedation on the laryngopharyngeal anatomic structures were assessed with a nonparametric Wilcoxon signed rank test. The effects of the head posture on the laryngopharyngeal anatomic structures were assessed with a Mann-Whitney U test and Kruskal-Wallis test. In all analyses, a value of P < 0.05 was considered significant. All data are reported as median (IQR) with the exception of the ICC test results, which are each reported with the 95% CI. For the study purposes, ICC values of < 0.5, 0.5 to 0.75, 0.75 to 0.9, and > 0.9 represent poor, moderate, good, and excellent reliability, respectively.15
Results
Among the 6 dogs, the order of evaluation of head posture was flexed, neutral, and then extended head posture for 2 dogs; flexed, extended, and then neutral head posture for 1 dog; neutral, extended, and then flexed head posture for 1 dog; and extended, neutral, and then flexed head posture for 2 dogs.
Intra-observer reliability
Analysis of the 3 measurements of TSP, DNL, OLES, and DET obtained by the 1 observer revealed that the ICCs were as follows: TSP, 0.975 (95% CI, 0.935 to 0.992); DNL, 0.966 (95% CI, 0.948 to 0.979); OLES, 0.993 (95% CI, 0.989 to 0.995); and DET, 0.940 (95% CI, 0.841 to 0.981). With regard to the evaluation of the laryngopharyngeal structures by 1 observer, the ICCs and their 95% CIs indicated that the reliability of the measurements was excellent for TSP, DNL, and OLES and good to excellent for DET (all P < 0.01).
Influence of the head posture on the ABN
Among the 6 dogs, the median ABN was 91.50° (IQR, 86.75° to 95.00°), 125.00° (124.50° to 125.50°), and 160.00° (160.00° to 163.50°) when head posture was flexed, neutral, and extended, respectively (Figure 3). During positioning of the dogs in the flexed, neutral, and extended head postures, the angle of the head was set at 90°, 125°, and 160°, respectively. There were no significant differences between the ABN and angle of the head when dogs had flexed, neutral, or extended head posture.
Influence of head posture on laryngopharyngeal structures
Measurements of TSP, DNL, OLES, and DET were each affected by head posture (Table 1). When dogs were sedated and positioned with a flexed head posture, the median maximal and minimal DNL and DET were each significantly (P < 0.05) decreased and the median maximal and minimal TSP were both significantly (P < 0.05) increased, compared with findings when dogs were positioned with a neutral head posture. With the extended head posture, the median minimal DNL and the median maximal and minimal DET were significantly (P < 0.05) increased and the median maximal and minimal OLES were significantly (P < 0.05) decreased, compared with neutral head posture findings. In addition, all the measured variables differed significantly (P < 0.05) when dogs were positioned with flexed versus extended head postures.
Maximum and minimum values of TSP, DNL, OLES, and DET determined from fluoroscopic images of 6 sedated Beagles positioned in right lateral recumbency with flexed, neutral, or extended head posture.
Variable | Value | Flexed head posture | Neutral head posture | Extended head posture |
---|---|---|---|---|
TSP (mm) | Maximum | 8.50 (7.25–9.58)a | 6.80 (5.38–7.30) | 5.25 (4.08–5.90)b |
Minimum | 8.05 (6.75–9.08)a | 6.25 (5.30–7.05) | 4.95 (4.05–5.83)a,b | |
DNL (mm) | Maximum | 3.75 (2.45–4.23)a | 11.85 (11.18–12.93) | 12.50 (11.25–13.33)b |
Minimum | 1.85 (1.30–2.50)a | 9.50 (8.65–10.33) | 11.35 (10.15–11.95)a,b | |
OLES (mm) | Maximum | 9.25 (8.80–9.78) | 8.60 (7.70–9.03) | 4.40 (3.53–6.13)a,b |
Minimum | 9.20 (8.75–9.35) | 8.30 (6.80–8.68) | 4.15 (3.30–6.03)a,b | |
DET (mm) | Maximum | 17.50 (16.45–18.20)a | 19.10 (17.80–19.95) | 23.30 (22.33–24.03)a,b |
Minimum | 17.15 (16.45–17.90)a | 18.80 (18.40–19.53) | 22.60 (21.30–23.53)a,b |
Data are presented as median (IQR).
For each dog, 3 head postures were established by manipulating the atlanto-occipital joint to alter the position of the head in relation to the neck. When the angles between the imaginary line drawn parallel to the ridge of the nose and the line drawn parallel to the dorsal ridge of the neck angle measured with a protractor were 90°, 125°, or 160°, the associated head postures were defined as flexed, neutral, and extended, respectively. To prevent head rotation, the muzzle of each dog was manually restrained and positioned so that the dog's tympanic bullae and mandibles overlapped on the fluoroscopy image. At least 3 regular respiratory cycles were observed for each head posture, where 1 respiratory cycle was defined as the interval between the beginning of one inspiration to just before the beginning of the next inspiration. Fluoroscopy videos were recorded at a frame rate of 30 frames/s. For each variable, the mean was calculated from values recorded for 3 respiratory cycles for each dog, and then the median was calculated for all 6 dogs.
Value is significantly (P < 0.05) different from that for the neutral head posture.
Value for the extended head posture is significantly (P < 0.05) different from that for the flexed head posture.
Influence of head posture on the PDNLD
The median PDNLD values were 44.35% (IQR, 41.73% to 49.30%; minimum value, 40.00%; maximum value, 57.14%), 20.40% (IQR, 19.40% to 22.18%; minimum value, 17.65%; maximum value, 25.11%), and 8.90% (IQR, 6.13% to 12.03%; minimum value, 3.17%; maximum value, 13.04%) when dogs were positioned with the flexed, neutral, and extended head postures, respectively. Compared with the median PDNLD when dogs were positioned with the neutral head posture, values were significantly (P < 0.05) increased and decreased when dogs' heads were flexed and extended, respectively.
Effect of sedation on the laryngopharyngeal structures in the neutral head posture
Data were obtained when the dogs were positioned with a neutral head posture, with and without sedation. There were no significant differences in median maximal and minimal TSP, DNL, OLES, or DET with or without sedation (Table 2). Overall, values were unchanged when dogs were in a conscious or sedated state.
Effect of sedation on the maximum and minimum values of TSP, DNL, OLES, and DET determined from fluoroscopic images of the 6 Beagles positioned in right lateral recumbency with a neutral head posture and with or without sedation.
Variable | Value | No sedation | Sedation | P value |
---|---|---|---|---|
TSP (mm) | Maximum | 6.55 (5.75–7.08) | 6.80 (5.38–7.30) | 0.715 |
Minimum | 6.40 (5.45–6.70) | 6.25 (5.30–7.05) | 0.786 | |
DNL (mm) | Maximum | 12.00 (11.45–12.88) | 11.85 (11.18–12.93) | 0.528 |
Minimum | 9.40 (9.00–10.28) | 9.50 (8.65–10.33) | 0.916 | |
OLES (mm) | Maximum | 8.80 (6.80–9.23) | 8.60 (7.70–9.03) | 0.498 |
Minimum | 8.70 (7.68–9.28) | 8.30 (6.80–8.68) | 1.000 | |
DET (mm) | Maximum | 19.10 (18.18–19.70) | 19.10 (17.80–19.95) | 0.345 |
Minimum | 19.55 (17.95–20.70) | 18.80 (18.40–19.53) | 0.600 |
A value of P < 0.05 is considered significant.
Fluoroscopic examination of the laryngopharyngeal structures was first performed with each dog manually restrained with a neutral head posture without sedation. Each dog was subsequently mildly sedated (medetomidine,c 0.015 mg/kg, IM), and fluoroscopic examination of the laryngopharyngeal structures with a neutral head posture was repeated.
See Table 1 for remainder of key.
Discussion
Fluoroscopy is a diagnostic imaging technique that is noninvasive, does not require anesthesia of examined individuals, and can detect in real time dynamic changes in the upper respiratory tract during the respiratory cycle. In dogs, the criteria for positioning the head to obtain an appropriate head angle for radiographic or fluoroscopic examinations had not been previously studied, to our knowledge. Because head posture affects the features and measurements used as diagnostic criteria for upper respiratory tract disease, any subjective interpretation of the effects of head posture needs to be avoided. In the present study, the ABN was measured to facilitate objective interpretation of the effects of the head posture on the upper respiratory tract fluoroscopic findings in dogs. No significant difference was found between the ABN and the actual positioned angle of the head in the various head postures. Therefore, the study results have suggested that the ABN can be used to verify head posture; because the appearance of laryngopharyngeal anatomic structures changes when the head is in a flexed or extended posture, ABN can be used to maintain a neutral head posture during fluoroscopic examination.
In the present study, different head postures resulted in measurable variations in laryngopharyngeal anatomic structures. The underlying mechanisms behind these anatomic changes in the upper respiratory tract in response to changes in head posture may be related to traction of the caudal portion of the trachea, compression of the upper airway extraluminal tissue space, and stretching of the pharyngeal airway.16,17,18 Extension of the atlanto-occipital joint increases the tracheal length and traction forces and decreases the compression of the upper airway extraluminal tissue space, which leads to a decrease in extraluminal tissue pressure and upper airway collapsibility. The increased DNL detected with the extended head posture may be associated with decreased extraluminal tissue pressure and increased upper airway patency. Changes in the upper airway corresponding to changes in head posture have been studied in humans12 and horses.13 With a flexed head posture, the upper airway narrows; conversely, with an extended head posture, the upper airway widens.12,13 The results of the present study in dogs indicated that the diameter of the pharyngeal lumen increases with an extended head posture, compared with that in a neutral head posture, a finding that was in agreement with those of previous studies.12,13 Changes in the TSP and OLES may also be related to extraluminal tissue pressure and the stretching of the pharyngeal airway. Further studies are needed to investigate the physiologic changes in the soft palate and epiglottis resulting from changes in head posture. Finally, in the present study, the flexed head posture–associated DET was decreased, compared with the neutral head posture–associated DET, which may have been attributable to dorsal displacement of the epiglottis as a result of a thickened soft palate.
Among the dogs of the present study, the PDNLD was observed to increase and decrease from the neutral head posture value when the head was flexed and extended, respectively. In the isolated upper airways of clinically normal animals, large changes in negative pressure trigger a dual protective reflex that restores airway patency by activating the airway dilators while inhibiting the electrical activity in the diaphragm, as has been detected by electromyography.3 Therefore, negative airway pressure alone does not cause pharyngeal collapse.19 However, upper airway patency decreases when the head is flexed and increases when the head is extended. Upper airway collapsibility also increases when the head is flexed and decreases when the head is extended.4 Therefore, the mechanism underlying the changes in the PDNLD associated with alterations in head posture may potentially be related to upper airway collapsibility and patency; when the head is flexed, the increased upper airway collapsibility and decreased upper airway patency increase the difference in the DNL during inspiration and during expiration.
Because the anatomic features and relationships of the laryngopharyngeal structures change with head posture, it is necessary to distinguish normal changes caused by variable head posture from abnormal changes caused by upper respiratory tract diseases. First, pharyngeal collapse is a condition in which the pharynx is completely or partially collapsed owing to dorsal displacement of the soft palate or ventral displacement of the dorsal pharyngeal wall.20 Further, pharyngeal collapse is defined as complete collapse when the pharyngeal lumen is 100% collapsed or as partial collapse when the pharyngeal lumen is > 50% but < 100% collapsed.5 In the present study, 1 of the 6 dogs had a PDNLD of 57.1% when positioned with the flexed head posture, which could have been mistakenly diagnosed as partial pharyngeal collapse. Second, an elongated soft palate is a condition in which the soft palate is longer than normal to the extent that it overlaps with the tip of the epiglottis.9 Among the dogs of the present study, the OLES was increased from the neutral head posture value when the head was in the flexed posture. With the extended head posture, the maximal and minimal OLES values were 4.40 mm (IQR, 3.53 to 6.13 mm) and 4.15 mm (3.30 to 6.03 mm), respectively, which confirmed that the soft palate was located behind the tip of the epiglottis. Diagnosis of an elongated or thickened soft palate is usually achieved through pharyngoscopic or laryngoscopic examination.21 However, these methods require a patient to undergo general anesthesia and are invasive. Although radiography and fluoroscopy are good methods for the diagnosis of an elongated soft palate given that the procedures are noninvasive and simple to perform, the radiographic criteria for diagnosis of an elongated soft palate do not take into consideration postural and breed-based differences. Therefore, further studies are required to develop more accurate diagnostic criteria for an elongated soft palate in dogs.
In veterinary medicine, sedation is indispensable when an animal is not cooperative, aggressive, or highly mobile during examinations. Further, sedation can be particularly important because positioning of the animal with accurate posture is important for fluoroscopic examination of the upper respiratory tract. In the present study, there were no significant differences in the laryngopharyngeal structure measurements obtained when the dogs were or were not sedated. Anesthetic agents, including medetomidine, reduce the respiratory rate and cause muscle relaxation; however, administration of medetomidine does not affect the laryngopharyngeal structures.22 Results of a previous study13 also indicate that sedation did not affect the radiographic pharyngeal diameter in 10 horses.
There were several limitations of the present study. A small number of dogs was included, and those dogs had minimal variations in their BCSs, ages, and weights. In humans and other animals, obesity is the main cause of increased pharyngeal fat accumulation and airway pressure through the area.23,24,25 In dogs, obesity also induces airway hyperreactivity by increasing the level of response to inhaled histamine.26 Therefore, compared with clinically normal dogs, dogs with high BCS or obesity are likely to develop changes in the geometry of the upper respiratory tract in response to different head postures. Also, the present study included only Beagles, which are mesocephalic dogs. In brachycephalic dog breeds, upper airway obstruction and increased airway resistance are induced owing to their craniofacial morphology.27 Therefore, further studies involving other dog breeds, such as brachycephalic dog breeds, with anatomic variations of the upper respiratory tract are required. Fluoroscopic examinations in the present study were conducted only when the dogs were in right lateral recumbency. Given that fluoroscopic examinations are also performed when animals are in sternal recumbency or a standing position,5,8 further research is needed to investigate any additional changes in the upper respiratory tract that may occur in association with sternal recumbent or standing positions. Finally, the present study did not investigate the effects of head rotation on the laryngopharyngeal structures. In dogs and humans, head rotation or oblique postures during lateral radiography result in image distortion, which affects cephalometric measurements or measurements of the upper respiratory tract.9,28 In addition, a previous study4 of humans revealed no significant difference in Pcrit between the neutral and rotated head postures. Therefore, quantitative evaluation of the effects of head rotation during fluoroscopy or radiography on measurements of the upper respiratory tract in dogs is needed.
The results of the present study have suggested that ABN is a useful variable for accurate evaluation of head posture during fluoroscopic examination for detection of upper respiratory tract diseases in dogs. In addition, it was confirmed through fluoroscopy that the anatomic features of the laryngopharyngeal structures and associated measurements (TSP, DNL, OLES, and DET and calculation of PDNLD) change dynamically, depending on head posture. These changes have highlighted the importance of distinguishing normal anatomic changes associated with head posture from abnormal changes caused by upper respiratory tract diseases, especially with regard to evidence of pharyngeal collapse or elongated soft palate. The recommendation is that fluoroscopic examinations to evaluate the upper respiratory system should be performed with dogs positioned with a neutral head posture to avoid inducing changes in the laryngopharyngeal structures associated with a flexed or extended head posture. Not only can ABN be used to maintain a neutral head posture during fluoroscopy, but also it can be used to standardize flexed and extended head postures for purposes of comparison. Further studies will be required to investigate the influence of head posture on the examination results of various dog breeds, including dogs with clinical signs of upper respiratory tract diseases.
Acknowledgments
This paper was supported by Konkuk University in 2018. The authors declare that there were no conflicts of interest.
Abbreviations
ABN | Angle between the basisphenoid bone and nasopharyngeal dorsal border |
BCS | Body condition score |
DET | Distance between the epiglottis and tympanic bulla |
DNL | Diameter of the nasopharyngeal lumen |
ICC | Intraclass correlation coefficient |
IQR | Interquartile (25th to 75th percentile) range |
OLES | Overlapping length between the epiglottis and soft palate |
Pcrit | Pharyngeal critical closing pressure |
PDNLD | Percentage difference in the nasopharyngeal luminal diameter |
TSP | Thickness of the soft palate |
Footnotes
REX-525RF, Listem, Gangwon, South Korea.
Research randomizer, Random.org, Randomness and Integrity Services Ltd, Dublin, Ireland. Available at: www.random.org.
Domitor, Pfizer Animal Health, Tadworth, England.
ImageJ, National Institutes of Health, Bethesda, Md.
Radiant, Medixant, Poznan, Poland.
SPSS, version 24.0, IBM Corp, Armonk, NY.
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