Abnormal shape of the pterygoid bone in French bulldogs: Prevalence and implication for cross-sectional area

Abstract

Objective

Retrospective observation of computed tomographic images to describe an anatomical difference in the shape of the pterygoid bone in French bulldogs (FB) and determine its prevalence and effect on the cross-sectional area of the airway, in comparison with normal conformation in brachycephalic and mesocephalic dogs.

Animals and procedure

Computed tomographic studies of FB and cocker spaniels (CS) that underwent examination of the head were reviewed. The shape and cross-sectional area of the pterygoid bone was recorded and compared between groups.

Results

Thirty-six CS and 34 FB were included. In 79.41% (27/34) of FB, there was an abnormal shape of the pterygoid bone in comparison with all 36 CS, which had a normal shape of the pterygoid bone. Only 20.58% (7/24) of FB had a normal shape. The cross-sectional area of the airway at the level of the pterygoid bone for FB was 88.78 mm². The area was larger in FB with normal shape (average: 95.70 mm², SD ± 15.98) than those with abnormal shape (average: 86.98 mm², SD ± 20.32), though this difference was not statistically significant (P > 0.05). Cocker spaniels had a larger airway cross-sectional area than dogs in both FB groups, with a mean of 142.28 mm² (± 24.87) and P < 0.05.

Conclusion and clinical relevance

French bulldogs frequently have an abnormal conformation of the pterygoid bone. This study identified further anatomical factors that might contribute to upper-airway obstruction in brachycephalic dogs.

INTRODUCTION

Brachycephalic dogs are characterized by an extreme developmental shortening of the craniofacial skull and nasal cavity, which leads to abnormal conformation of the nasopharyngeal structures that can cause brachycephalic obstructive airway syndrome (BOAS) (1–5). Classic conformational changes include an elongated soft palate, stenotic nares, everted laryngeal saccules, and rostral and caudal aberrant nasal turbinates (1,4,6–8), but an increasing number of specific anatomical differences between brachycephalic and mesocephalic dogs have been identified (1–3,5–7,9–15). Additional reported abnormalities include laryngeal collapse (6,9,16), hypoplastic trachea (6,7,10,16), macroglossia (11,17), dorsal rotation of the maxillary bone (1,18), vocal fold granulomas (19), nasopharyngeal mucoceles (9), and partial collapse of the left mainstem bronchus (9,10). The roles of different anatomical regions and combinations of different abnormalities in the development and severity of BOAS are still not fully understood; therefore, postsurgical outcomes are difficult to predict (3,13,16,17,20–23).

Current surgical options attempt to alleviate respiratory obstruction and can provide significant improvement, with studies showing that 60 to 90% of dogs have improved clinical signs following airway surgery (3,9,21). However, < 1/2 of these cases are considered to have “excellent” outcomes, defined as BOAS Grade 0 or Grade I after surgery (3,13,21), as 60 to 70% of brachycephalic dogs have ongoing compromised respiratory function. Identification of those individuals that will have excellent outcomes after surgery remains difficult (21,24,25). The limitations of surgical treatment and welfare concerns have driven interest in the development of strategies to identify dogs that are suitable for breeding, in order to develop a population of brachycephalic dogs that are minimally affected by BOAS (26).

Over the last decade, computed tomography (CT) has become the key imaging modality for the diagnosis of upper-respiratory abnormalities, including BOAS. Computed tomography allows assessment of relevant anatomical landmarks, symmetry, presence of airway obstruction, and other structural abnormalities without superimposition of bone and soft tissues (2,5,7,11,13,14,20,27–32). The severity and range of clinical signs are difficult to quantify with diagnostic imaging, leading to the development of functional examination methods, such as functional exercise test grading system, endoscopy, and plethysmography, to allow a more accurate grading of BOAS severity (2,5,7,10,12,20,24,26,33). Functional testing in mesocephalic dogs showed that most of the airway resistance during inspiration arises in the nasal cavity. Equally, it was shown that narrowing or obstruction of the nasopharynx in brachycephalic dogs contributes to severe airflow restriction, resulting in typical clinical signs (1,3,8,10,20). Breathing patterns assessed by tidal breathing flow-volume loops showed that most brachycephalic dogs suffer from a fixed type of upper-airway obstruction related to conformational obstruction in the nasopharynx (10,24,25,33).

When observing the nasopharynges of brachycephalic dogs, the authors noticed that, in CT studies, many showed a medial deviation of the wings of the pterygoid bone (Pt) compared to mesocephalic dogs, resulting in latero-lateral narrowing of the airway. At this level, the bone structure surrounds the nasopharynx laterally and dorsally, which means that the airway cannot be modified by muscle contraction during the breathing cycle as it is more caudally (9).

This study was designed to determine the prevalence of medial deviation of the Pt wings in French bulldogs (FB) and cocker spaniels (CS) (representing a mesocephalic dog breed), and to characterize the airway implication of the abnormal shape in FB dogs compared to mesocephalic dogs. The authors conducted a search of online databases from Elsevier, ScienceDirect, PubMed, and Google Scholar, using the keywords “brachycephalic,” “pterygoid bone,” “shape,” and “nasopharynx,” and no studies referring to the anatomical features of the Pt in brachycephalic dogs were identified. The 1st hypothesis was that this abnormal shape was a common finding in FB and present only in this group. A 2nd hypothesis was that the area of the nasopharynx was larger in FB with normal conformation of the Pt compared to FB with abnormal conformation of the Pt. In addition, a 3rd hypothesis was that the area of the airway in CS was larger than in FB, regardless of the conformation.

MATERIALS AND METHODS

Study population

A search of a small animal hospital’s database was carried out to identify all FB and CS presented between March 2016 and October 2020 that had a CT examination of the head under general anesthesia and with an endotracheal tube in place. Clinical records and CT studies were retrospectively reviewed. Dogs were divided into 2 populations (FB and CS) according to signalment. Exclusion criteria were cases with previous surgery of the upper airway or structural diseases in the soft tissue or bone surrounding the Pt, or cases where there was no recorded consent for data use by the owner. Dogs with nasal disease were not excluded from the study if there was no destruction of any anatomical structures and no caudal extension of the disease into the nasopharynx.

Computed tomographic acquisition and examination

Computed tomography of the head was acquired following the local protocol, with the head resting on a positioning block, in spiral mode, with either a helical 2-slice scanner (HiSpeed Dual; GE Medical Systems, Buckinghamshire, UK) or 64-slice scanner (Somatom Perspective; Siemens Healthcare, Surrey, UK), with a slice thickness of 1 mm and slice reconstruction interval of 0.5 mm. Multiplanar reconstructions of the CT study were examined, using a high-frequency reconstruction algorithm and a bone window (window level: 300 and window width: 1500).

The images were reconstructed with image-viewing software (Horos; Horos Project, Brooklyn, New York, USA). The dorsal plane was aligned parallel to the hard palate, the sagittal plane was aligned parallel to the midline, and the transverse plane was always orthogonal in relation to both other planes (Figure 1 A, B, C). The resulting transverse images displayed the ultimate plane to accurately evaluate the airway in the location Pt. The “location Pt” was defined as the most caudal slice where the Pt could be seen completely; the next caudal slice would not show the wings of the Pt integrally. A Board-certified radiologist (PA) and a Board-certified surgeon (DA) validated the technique, and the same investigator (MB) made all the measurements in the bone window.

FIGURE 1.

Determination of location Pt. A — Plain (non-contrast) sagittal reconstruction from the computed tomographic study of a cocker spaniel dog. The orthogonal axes are first centered on the dorsal aspect of the nasopharynx, with the blue line as parallel as possible to the palatine bone. B — Dorsal planar reconstruction from the same study. The yellow line is placed as parallel as possible to the midline. C — Cross-sectional transverse reconstruction image from the same study, resulting from the axes adjustment in (A) and (B). On the cross-sectional view, we choose the most caudal slice that allows vision of the pterygoid wing in its integrity. The next slice caudally will not show the wings of the pterygoid bone integrally.

Pt — Pterygoid bone.

Classification and comparison of the pterygoid bone shape

The shape of the Pt in location Pt was assessed as illustrated in Figure 2; it was classified as normal if the widest latero-lateral measurement was mid-height of the nasopharynx (Figure 2 A); or as abnormal if the widest point of the airway coincided with the dorsal aspect of the airway, indicating medial deviation of the Pt wings (Figure 2 B).

FIGURE 2.

Selection of normal versus abnormal conformation of pterygoid bone. A — Plain transverse reconstruction from the computed tomographic study of a dog with normal pterygoid bone shape. The widest point is mid-height of the nasopharynx (blue line), ventral to the dorsal aspect of the nasopharynx (red line). This was designated a “normal shape.” B — Plain transverse reconstruction from the computed tomographic study of a dog with abnormal pterygoid bone shape. The widest point coincides with the dorsal aspect of the airway (purple line). This was designated an “abnormal shape.”

Comparison of the area of the airway at the level of the pterygoid bone between normal and abnormal shape for each breed

The area of the airway at Pt was directly compared between shapes and groups. The measurements were determined freehand, in mm², using a cursor; and were subsequently calculated by CT software, in mm for distances and mm² for areas, in cross-section of the location Pt.

Statistical analysis

The data were analyzed to determine if the hypotheses were valid. For all variables, a Kolmogorov-Smirnov test (with Lilliefors correction) was used to confirm that the data were normally distributed in both groups. The 1st analysis for the variable “shape” was expressed in percentages of normal and abnormal shapes. The 2nd analysis was conducted to determine if the cross-sectional area in location Pt was shape-dependent and/or breed-dependent. A X² test was used to confirm a normal distribution. A Welch t-test was used to test the correlation between the area and the breed and the area and the shape.

RESULTS

Study group

The FB group comprised 34 client-owned, purebred FB. Ten FB were female and 24 were male. The median age was 2.5 y (7 mo to 12 y) and median weight was 12.3 kg (7.3 to 17.2 kg). The CS group comprised 36 client-owned, purebred CS. Sixteen dogs were female and 20 were male. Median age was 7 y (1 to 15 y) and median weight was 13.9 kg (9.7 to 20.9 kg). There were no significant differences in sex, body weight, or age between the 2 study populations (P < 0.05).

Study of the shape of the pterygoid bone

All 36/36 CS (100%) had a normal shape of the Pt, and only 7/34 FB (20.58%) had a normal shape of the Pt. The remaining 28 FB (79.41%) had an abnormal Pt shape.

Study of the cross-sectional area of the airway

Using the Kolmogorov-Smirnov test with Lilliefors correction, the cross-sectional area at location Pt was confirmed to follow a normal distribution. The mean cross-sectional area at location Pt for FB was 88.78 mm² with standard deviation ± 19.61 mm², and for CS was 142.28 mm² with standard deviation ± 24.87 mm². The mean area for the 7 FB with normal Pt was 95.70 mm² with standard deviation ± 15.98 mm², and the 28 FB with abnormal Pt had an average area of 86.98 mm² with standard deviation ± 20.32 mm².

The difference in airway areas was not statistically significant between the 2 FB shape groups (P = 0.25). The difference in airway areas was statistically significant between CS and FB groups, regardless of the shape (P = 6.988 × 10⁻¹⁵).

DISCUSSION

This study provided evidence that the shape of the Pt was abnormal in the majority of a population of FB evaluated for medial deviation of the wings of the Pt. This anatomical abnormality was a common finding in the brachycephalic group in this study and was not present in the mesocephalic group. This fact allowed us to accept our 1st hypothesis. This difference in the shape of the Pt has not been previously described in the literature, despite its high prevalence of almost 80%.

The 2nd hypothesis was rejected, as the difference between normal and abnormal shapes of the Pt did not seem to have a statistically significant effect on the airway area at this level. Surprisingly, the shape of the Pt aperture did not seem to have an effect on the size of the nasopharyngeal airway, despite the Pt surrounding the airway dorsally and laterally, and many studies showing the effects of conformational variations of the nasal and nasopharyngeal lumen on functionality (10,25,33,34). We consider the possibility of a statistical error due to the small sample of normal FB. The 3rd hypothesis was accepted, as both FB groups had much smaller areas than CS, regardless of the shape.

The narrowest area of the nasopharynx in brachycephalic dogs is the caudal aspect at the end of the soft palate (1,2,15,20), making this area the focus of most studies on nasopharyngeal obstruction of airflow in brachycephalic dogs. This caudal narrower area is surrounded by soft tissue, and conscious control of the pharyngeal muscles can maintain patency at this level during the respiratory cycle (9). In our area of study, there is rigid bone dorsally and laterally, and the soft palate ventrally has limited mobility, preventing the ability to consciously modify airway patency. This physical and unchangeable anatomy affecting the upper-airway resistance of brachycephalic dogs is an important concern when considering the available surgical techniques to modify upper-airway resistance in dogs affected by BOAS. As this location cannot be consciously or surgically modified, a local narrowing could have negative clinical consequences, affecting the outcome of any current corrective surgery technique (3,9,17,21). This could account for the variability in clinical improvement following corrective surgery. To the best of our knowledge, there are no studies describing experimental or clinically applied techniques of surgical correction for Pt abnormalities in dogs.

When studying the Pt and associated airway at this location, previous studies of the nasopharynx of brachycephalic dogs used a cross-sectional measurement at the caudal tip of the hamulus of this bone (11,35). However, our area of study was slightly more rostral in order to describe the shape of the Pt and evaluate the effect on the luminal area.

We know that the nasopharynx varies between different brachycephalic breeds (11,18). A recent study comparing tongue areas between brachycephalic breeds also included measurements of the nasopharynx (11). The conclusion was that the pug had a significantly smaller nasopharyngeal area than 2 bulldog breeds at the level of the Pt, making variations or abnormalities in shape potentially more significant for this breed (11). The rest of the nasopharyngeal measurements rostral and caudal to this point did not differ significantly between brachycephalic breeds (11). However, no comparison with mesocephalic breeds was carried out and the studies did not examine shape of the Pt. In our study, the FB was selected as a model because inter-breed variations are reported to be minimal (11,18) and this breed is routinely scanned in our hospital for BOAS.

It is unclear if our findings in FB also apply to other brachycephalic dog breeds, and further studies to determine if the shape of the Pt differs between brachycephalic breeds would be necessary to complete the existing data on the nasopharyngeal airway cross-sectional shape. The CS was chosen as a model for mesocephalic breeds due to similarity in weight and skull width, allowing direct comparisons between normally distributed groups.

Many anatomical aspects of the upper airway, such as the soft palate or the BOAS functional grade, were not investigated in this study. It was not our objective to correlate the physical findings to functional testing, such as exercise testing or whole-body barometric plethysmography (10,20,24,26,33,34), and the clinical effect of the rigid structural abnormalities we describe is theoretical. Further research to correlate Pt shape with conscious functional testing could be useful, particularly to provide an objective tool for prognostic indicators or breeding criteria.

Limitations of this study included the retrospective use of CT studies. Ideally, the imaging should have been done without endotracheal intubation, as intubation can lead to dorsal displacement of the soft palate; however, this approach is not without risk in sedated or anaesthetized brachycephalic dogs and is not the policy in our hospital (9,35). In this study, to minimize this variable, measurements were taken in areas not thought to be influenced by the presence of an endotracheal tube, and all dogs in both groups were intubated (5,35).

In conclusion, the majority of FB showed an anatomical variation of the anatomy at the level of the Pt. This abnormal shape seems not to have a statistically significant effect on the area of the airway at this point. Regardless of the shape of the Pt, FB had a significantly smaller airway area than dogs in the mesocephalic group at this location. The correlation of these findings with the severity of BOAS grading and surgical outcome is required to establish the significance of the pterygoid abnormalities. CVJ