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Brachycephalic Upper Airways Syndrome
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Brachycephalic breeds are usually distinguished from mesocephalic and doliocephalic breeds by their shortened skull, which is a result of early ankylosis of the skull cartilages. Brachycephalic breeds have been defined by different measurements [1,2]: A skull width to length ratio greater than 0.81, a face to skull ratio of 1.6 to 3.44, or a craniofacial angle less than 14° (angle between the base of the skull and the facial skull). Breeds usually recognized as brachycephalic by these definitions include: Boston terrier, English and French bulldog, pug, Pekinese, Shi-tzu, and Cavalier King Charles. Some miniature breeds as Yorkshire terriers and miniature pinschers are also often included in this list.
Upper respiratory syndrome has been described in brachycephalic dogs (BD). Clinical signs usually include snoring, inspiratory dyspnea, exercise intolerance, stridor, cyanosis, or even syncopal episodes in more severe cases. These problems are usually aggravated with stress, exercise, or heat. Labored breathing is accompanied by over dilatation of the chest, because a higher intrathoracic negative pressure tends to suck the abdomen into the thoracic cavity. The upper respiratory syndrome usually becomes more severe with increasing age. Vomiting or regurgitation of saliva is also frequently encountered in association with this syndrome.
Anatomy of the Upper Airways in Brachycephalic Dogs
Several anatomic abnormalities can be found in the brachycephalic dog [1-3]. The cartilaginous skeleton of the external nares is usually shorter, thicker, and medially displaced compared with non-brachycephalic breeds, causing secondary obstruction of the nostrils. Owing to shortening of the skull, the size and shape of the conchae are modified, leading to potential intranasal stenosis. The transition from hard to soft palate is usually caudal to the last molar in dolichocephalic and mesocephalic breeds, whereas it is more caudally located in BD. The soft palate, which normally extends to the top of the epiglottis, can extend up to 1 to 2 cm beyond the epiglottis and can be readily aspirated into the rima glottidis during inspiration. On radiographic examination (Fig. 51-1 and Fig. 51-2) one can readily see that, in BD, the soft palate is not only overlong but also over-thick [4]. In many BD, especially French and English bulldogs, the base of the tongue is also hyperplastic; the term macroglossia has usually been used to define this abnormality. Besides these findings, other tissue redundancies can be found, especially in the oro- and nasopharynx region.
Figure 51.1. Lateral radiograph of pharyngeal region of a mesocephalic dog. The oro- and nasopharynx can be readily seen as two broad stripes of aeric density.
Figure 51.2. Lateral radiograph of pharyngeal region of a brachycephalic dog. The two broad stripes of aeric density have disappeared and the soft palate appears both elongated and thickened.
The rima glottidis, the narrowest airflow passage of the upper airways, is formed by the paired arytenoid cartilages and the vocal folds. The laryngeal saccules, or ventricles, are located cranial to the vocal folds and cannot be seen in a normal dog. In many BD, the laryngeal ventricles can be seen protruding into the laryngeal lumen [5]. Owing to an abnormal embryogenesis, the trachea of some brachycephalic dogs (mainly English bulldogs) is hypoplastic, which further decreases the upper respiratory airflow [6].
These anatomic anomalies are responsible for a multifocal obstruction of the upper-airways. The nostrils are narrowed by medially displaced nares, the nasopharynx and the oropharynx are "blocked" between a hyperplastic tongue and an overthick soft palate, and the rima glottidis is obstructed by the overlong soft palate. These anatomic abnormalities have secondary adverse functional consequences on laryngeal function.
Pathophysiologic Consequences
Brachycephalic dogs must produce higher negative pressure to breathe properly given their narrowed nostrils and nasal passages. During inspiration, the soft palate flutters into the rima glottidis and can even obstruct it. In some instances when negative pressure is high enough, it may exceed the natural resistance of the tissues, causing their collapse. This can be observed clinically in the nostrils and also in the larynx. The cuneiform and corniculate cartilages are drawn into the glottal opening following increased inspiratory efforts, causing laryngeal collapse. In these cases, an inspiratory stridor and even suffocation can be observed. In such patients the laryngeal ventricles are usually everted into the laryngeal lumen. Everted laryngeal ventricles and laryngeal collapse are secondary events that lead to even more severe respiratory compromise [2,5,7].
Other Findings in Brachycephalic Dogs Suffering from Upper Airway Compromise
Many owners describe signs of regurgitation or vomiting when their BD becomes excited or suffers respiratory distress [7-9]. In these instances, signs of respiratory distress are usually relieved when the dog vomits or regurgitates large packs of "foam." In one study on 73 brachycephalic dogs suffering from upper airway syndrome [9], respiratory and digestive signs were graded as minimal (grade 1), moderate (grade 2), or severe (grade 3), according to their frequency and severity. Respiratory signs were moderate in 20 dogs (27.4%) and severe in 51 (69.9%). Nineteen dogs (26%) were presented with grade 1 digestive disorders, 19 (26%) with grade 2, and 35 (48%) with grade 3. Among the 35 dogs with grade 3 digestive signs, 28 (80%) suffered from grade 3 respiratory disorders, 5 (14.3%) from grade 2, and 1 (5.7%) from grade 1. A correlation between the severity of gastric and respiratory signs was demonstrated (p=0.059).
Diagnosis
Several steps should be undertaken in order to make an accurate diagnosis of brachycephalic syndrome.
History And Clinical Signs
The history usually describes snoring and progressive exercise intolerance aggravated by warm temperature when the dog is 1 to 2 years old [5,9,10]. Therefore, most owners become aware of the problem during the second summer of the dog's life [7,9,11]. Unfortunately, because snoring is considered a normal respiratory feature of BD by most owners, breeders, and even practitioners, no further diagnostic or therapeutic steps are usually undertaken. With time, the condition worsens until signs of laryngeal collapse occur (inspiratory stridor). In these cases, most owners spontaneously find a way to open their pets' upper airways by opening the mouth and pulling the tongue forward. Concomitantly, vomiting or regurgitating food or saliva usually happens and this is also considered to be a normal feature of BD in most owners' and breeders' minds.
Radiographic Examination
Radiographic examination of the head can be used to assess the length and thickness of the soft palate. It can often be observed that both oropharynx and nasopharynx are equally compressed by mucosal hyperplasia (Fig. 51-1 and Fig. 51-2). Thoracic radiographs are recommended in order to diagnose hypoplastic trachea, aspiration pneumonia, and/or secondary right-sided heart failure [2,11].
Endoscopy
Given the common involvement of upper airways and the upper gastrointestinal tract, endoscopy should be conducted as part of a basic diagnostic work-up.
Length and thickness of the soft palate are assessed and, after removal of the endotracheal tube, the motion of the arytenoid cartilages and position of the ventricles are evaluated. In some cases, especially in very small brachycephalic dogs (e.g., pugs or Pekinese) the arytenoid cartilages are flaccid and have a tendency to rotate inward into the laryngeal lumen [7]. During the same procedure, upper gastrointestinal endoscopy is done. The esophagus, cardia, stomach, pylorus, and duodenum are evaluated. Gastric and duodenal biopsies are recommended [7-9].
Macroscopic and Endoscopic Findings
Stenotic nares and soft-palate hyperplasia are the two most common anomalies (present in 50 to 85% and 96 to 100% of cases, respectively [5,8,10,11]. Everted ventricles are usually found in 54 to 60% of cases [10,11] and although more rarely mentioned in the past [5,11] a moderate to severe laryngeal collapse was present in 64% (39/61) of the patients in a retrospective study [9].
Although many anatomic malformations of the gastrointestinal tract have been described in BD [12-15], some authors specifically studied digestive disorders in BD affected by upper airway compromise [7-9]. In one such study [9] 71 of 73 dogs (97.2%) were presented with esophageal, gastric, or duodenal anomalies. Forty-four dogs suffered esophageal anomalies; 12 presented with an esophageal deviation, 28 had cardial atony, 23 had gastroesophageal reflux, 3 had axial hiatal hernia and 27 had distal esophagitis. Chronic vomiting, slow gastric emptying, and hiatal hernias have been classically described to explain gastroesophageal reflux [16]. In brachycephalic breeds, a possible explanation is the high positive abdominal pressure generated by recurrent vomiting as well as the negative intrathoracic pressures generated by increased inspiratory work [17-21]. In the same study [9] among the 71 dogs suffering gastric anomalies, 65 presented with diffuse inflammation of the body or antrum and a punctiform inflammation was seen in 28 dogs; 23 presented with gastric stasis, 63 with pyloric mucosal hyperplasia, 22 with pyloric stenosis, 4 with pyloric atony, and 6 with duodenogastric reflux. A chronic diffuse or follicular gastritis was found in 50 of 51 specimens (98%). Gastritis was histologically graded as minimal in 13 cases (26%), moderate in 25 cases (50%), and severe in 10 cases (24%).
Gastrointestinal and Respiratory Signs: A Common Pathophysiologic Pathway
Gastroesophageal reflux associated with regurgitation and vomiting can contribute to upper esophageal, pharyngeal, and laryngeal inflammation. These phenomena have been documented experimentally in animals [22] and clinically in infants [23]. They can further contribute to upper respiratory problems. In turn, respiratory distress could stimulate the autonomous sympathetic nervous system, which would slow gastric motility and increase the gastric emptying time. Furthermore, the dilated antrum would stimulate gastrin-producing cells responsible for muscular hyperplasia [13,24]. In a study in exercising racehorses, the pressure over the lower esophageal sphincter was shown to be related to the obstruction of upper respiratory tract [25]. In humans, a high prevalence of hiatal hernia and gastroesophageal reflux has been demonstrated in asthma patients [26]. Finally, in the dog several cases of gastroesophageal diseases or hiatal hernia have been described associated with upper airway obstruction. [7-9,26,27]. The correlation between respiratory and digestive disorders suggests the influence of upper respiratory tract diseases on gastroesophageal diseases, and vice versa. The gastroesophageal disorders, ptyalism, regurgitation, vomiting, and reflux, can aggravate the respiratory signs by encumbering the pharyngeal region and stimulating persistent inflammation. Conversely, chronic respiratory depression promotes gastroesophageal reflux. The close relation between respiratory and digestive problems is sustained by the fact that most of these animals "vomit" large packs of saliva when excited or stressed or during respiratory distress.
Treatment
Early Relief of Respiratory Compromise
According to the pathophysiology of the syndrome, early relief of the proximally located obstruction should be attempted because it is postulated that early correction could prevent or even reverse ventricular eversion or laryngeal collapse [5]. Therefore, as soon as snoring is observed, rhinoplasty and palatoplasty are recommended. This has been done as early as at six months of age but the value of an earlier rhinoplasty is still debated.
Medical Treatment of Gastroesophageal Disease
The influence of surgical treatment of the upper airway on improvement in gastrointestinal signs has also been studied [28]. In this study, when an inflammatory gastrointestinal disease was observed endoscopically, a medical treatment, based on inhibition of hydrogen ion secretion (omeprazole 0.7 mg/kg per os every 24 hours) and prokinetic medication (cisapride 0.2 mg/kg per os every 8 hours), was recommended immediately after surgery. If distal esophagitis was noted, an antacid was prescribed for 15 days (magnesium hydroxide, 1 ml/kg per os after meals). Following histologic results, medical treatment was adjusted for each case. For moderate to severe gastritis, a 2-month course of treatment was recommended, including an inhibitor of hydrogen ion secretion (omeprazole, 0.7 mg/kg per os every 24 hours), a prokinetic (cisapride, 0.2 mg/kg per os every 8 hours), a surface protector (sucralfate, 1 g per os every 12 hours apart from the meals). For severe gastritis and/or duodenitis with parietal fibrosis, the same treatment was advised for 3 months and corticosteroids were added (prednisolone starting at 0.5 mg/kg per os every 12 hours).
This study also suggested that, after surgical treatment of the upper airways and despite discontinuation of medical treatment in more than 80% of the cases, a clear improvement of upper gastrointestinal tract disease was observed. In the cases where a control gastroesophageal endoscopy could be obtained six months after upper airway surgery, it always showed a complete resolution of the gastroesophageal endoscopic and histopathologic signs. These findings support the previous hypothesis of a common pathophysiologic pathway for upper respiratory and upper gastroesophageal disease in brachycephalic dogs.
Surgical Treatment
Nostrils
Several techniques of rhinoplasty have been developed [2,5]. They all aim at opening the lateral wings of the nostrils. Removing this part increases the diameter and contributes to improvement of the nasal airflow.
Elongated and Hyperplastic Soft Palate
Current techniques for treatment of elongated soft palate involve excision of the elongated part [2,5]. Although the level of excision has been recommended to be somewhere between the midpoint and the end of the tonsils, it is also considered wise to cut the soft palate at a level where it just comes into contact with the tip of the epiglottis. A new technique of palatoplasty, the so-called "Folded flap palatoplasty," has been developed to address both the pharyngeal and the laryngeal obstruction [4]. This technique achieves a marked reduction of the thickness of the soft palate, thereby relieving the nasopharynx and oropharynx from obstruction. As with the conventional techniques, the soft palate is shortened and the laryngeal obstruction is also relieved.
Laryngeal Collapse
In one study,9 64% (39/61) of the patients were presented with moderate to severe laryngeal collapse and 54% (33/61) with everted ventricles. Because it is postulated that laryngeal collapse and ventricular eversion are secondary events most likely a result of increased respiratory depression, relief of proximal obstruction should alleviate signs of laryngeal collapse. This has been observed clinically. In this study, only 1 dog out of 61 had laryngeal surgery (arytenoid lateralization) and 1 had an oral ventriculectomy. Although ventriculectomy has been recommended as a treatment for ventricular eversion, it increases local inflammation and can result in laryngeal webbing. Its benefit in improving clinical signs has not yet been proven. To the contrary, in a retrospective study looking at dogs with ventricular eversion, the overall prognosis was better in those that did not have a ventriculectomy [10].
Treating laryngeal collapse remains challenging. In cases where clinical signs are not improved after rhinoplasty and palatoplasty, lateralization of one of the arytenoid cartilages can be attempted. This usually provides an adequate laryngeal opening in cases where the cartilage is stiff enough. In some cases, the arytenoid cartilages are flaccid and have a tendency to invert into the laryngeal lumen. In our experience, these dogs do not respond favourably to lateralization and a permanent tracheostomy should be recommended.
Prognosis
Following this overall medicosurgical protocol, the prognosis 6 months after surgical treatment was graded as good in 22% and excellent in 67% of the cases [29]. Results with this protocol compare favorably with previous studies conducted at the same institution not accounting for gastroesophageal treatment [10].
Conclusion
In brachycephalic breeds, anatomic anomalies of the upper respiratory tract (i.e., stenotic nares and over-long and over-thick soft palate), progressively lead to further impairment of breathing owing to progressive laryngeal compromise (i.e., laryngeal collapse and ventricular eversion). In addition, gastroesophageal disease can be found clinically, endoscopically, and histologically in many brachycephalic dogs suffering from upper airway impairment. To relieve the upper airway obstruction, an early surgical treatment of the stenotic nares and of the over-long and over-thick soft palate is recommended. A concurrent medical treatment of gastroesophageal signs has also been shown to improve the overall prognosis.
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1. Chaudieu G, Denis B. Génétique des races canines dites brachycéphales. PMCAC 5:571-576, 1999.
2. Koch D, Arnold S, Hubler M, Montavon P. Brachycephalic syndrome in dogs. Compendium 25:48-55, 2003.
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1Clinical Department of Small Animals and Horses, Veterinary University, Vienna, Austria. 2Clinique Frégis, Arcueil, France.
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