Stenotic Nasopharyngeal Dysgenesis in the Dachshund: Seven Cases (2002–2004)
Medical records of seven dachshunds with congenital nasopharyngeal stenosis from abnormally thickened palatopharyngeal muscles were reviewed. The intrapharyngeal ostium in all cases consisted of only a narrow slit. Dogs were presented with various clinical signs—the most common being dyspnea, expiratory cheek puff, salivation, pharyngeal dysphagia, oral dysphagia (to a lesser extent), and macroglossia. Diagnostic procedures included direct pharyngeal inspection, pharyngeal and thoracic radiography, fluoroscopy, lingual ultrasonography, biopsies in two dogs, and a postmortem examination in one dog. Diagnoses were readily made with radiographs and visual examinations. Macroglossia was confirmed with transcutaneous ultrasonography or a transmandibular finger test.
Introduction
The pharynx is the proximal end of the respiratory and digestive tubes and is divided into three parts: the nasopharynx, the oropharynx, and the laryngopharynx. The nasopharynx is located dorsal to the soft palate and is delineated rostrally by the choanae and caudally by the intrapharyngeal ostium.1,2 Dorsally the nasopharynx is bound by the base of the skull and the muscles that attach to it.2 The oropharynx is bound dorsally by the soft palate and palatopharyngeal arches, ventrally by the root of the tongue, and laterally by the tonsillar fossae.1 The oro- and nasopharynx communicate with the laryngopharynx, and all structures open and close in a coordinated fashion during swallowing and respiration.1,3
Nasopharyngeal stenosis is defined as an obliteration of the normal communication between the nasopharynx and oropharynx. In companion animals, this stenosis mostly affects the rostral nasopharynx.4–10 Nasopharyngeal stenosis secondary to choanal atresia has been described in a 20-month-old shih tzu.11 The stenosis arose from a connective tissue membrane causing total choanal blockage on the left side and partial obstruction on the right side. Nasopharyngeal stenosis from fibrotic web formation has also been reported in two dogs and one cat.4 In the two dogs, the stenosis was a postsurgical complication after tumor removal.4 The pathogenesis of the web formation in the cat was unknown.4 Nasopharyngeal stenosis in cats may sometimes be caused by a thin, tough inflammatory membrane that develops across the rostral nasopharynx and results in a small, round nasopharyngeal opening.5–8,10 The postulated etiology in these cases is nasopharyngeal mucosal ulceration secondary to viral or bacterial rhinotracheitis.5,8 Dysphagia was not a presenting sign in any of the above nasopharyngeal conditions, as the pathology was located rostrally in the nasopharynx.5–8,10
In small animals, radiography and cross-sectional imaging techniques of the nasopharynx are important diagnostic tools for evaluating this area, but the use of radiographs in the diagnosis of nasopharyngeal stenosis has been questioned.4 Radiographic visibility of the stenotic membrane has only been described in one cat, in which a strand-like, soft-tissue opacity was visible across the nasopharynx on lateral views. The defect was confirmed with positive-contrast rhinography and magnetic resonance imaging.10 The only other radiographic change described in a cat with nasopharyngeal stenosis was a slight dorsal deviation of the soft palate at the level of the inflammatory membrane.7
The purpose of this study is to document a syndrome of nasopharyngeal dysgenesis in the dachshund, including clinical presentation, diagnostic methods, treatment outcomes, and possible etiologies. Only one prior case report of nasopharyngeal dysgenesis in the dachshund has been described.12
Materials and Methods
The medical and diagnostic imaging records of the Onderstepoort Veterinary Academic Hospital and Cape Animal Medical Center were reviewed for dogs that were presented with nasopharyngeal dysfunction from January 2002 through March 2004. The diagnosis of nasopharyngeal dysgenesis was based on pharyngeal radiographs and direct visualization of the defect. Data evaluated included signalment, clinical signs, findings from a visual pharyngeal inspection, results of a transmandibular finger test, pharyngeal and thoracic radiographs, swallowing videofluoroscopy, lingual ultrasonography, histopathology, and any surgical procedures performed.
The transmandibular finger test technique was developed to crudely assess lingual muscle hypertrophy by placing the index finger transversely across the ventral mandible at the level of the commissure [Figure 1]. In normal dachshunds, only the bones of the mandibular rami touch the finger. Lingual muscle hypertrophy causes bulging of the muscles against the finger in this region and prevents the mandibular rami from contacting the finger.
Percutaneous ultrasonography of the base of the tongue was performed in affected dogs and in three normal, smooth-haired dachshunds for comparison. Ultrasound measurements were made sagittally along the median sulcus at the thickest point.
Results
Clinical Findings
Seven cases fit the criteria for nasopharyngeal dysgenesis and included four male and three female smooth-haired dachshunds [Table 1]. Mean age of the dogs at presentation was 36 months (range 12 to 60 months). When the dogs were first seen at the referral center, their clinical signs had been present for 4 to 24 months (mean 12 months). The first clinical signs described by most owners were coughing and retching. Initially, these signs occurred only during eating, but later they were noted between meals as the condition progressed. Most dogs had only a poor or temporary response to various conservative therapies, such as antibiotics.
At presentation, an expiratory cheek puff seen during closed-mouth breathing was the most striking clinical sign. It occurred either continuously in severe cases (n=3) or only when the dog became excited or was exercised (n=4). Other clinical signs included occasional open-mouth breathing (n=2), inspiratory stridor (n=4), and hypersalivation (n=2). Progressive dysphagia was noted in all dogs and varied in severity. In some dogs, the dysphagia occurred only when eating dry pellets; in other dogs, it was also seen when drinking water. One dog had chronic-intermittent regurgitation and was diagnosed with an esophageal hiatal hernia. The pharyngeal pathology was discovered incidentally while the dog was under general anesthesia for placement of a gastric tube to repair the hernia.
On clinical examination, most dogs were in good body condition. Examination of the oral cavity revealed thickening of the base of the tongue (n=5), with vascular engorgement around the base in two cases. The transmandibular finger test (n=6) was positive in five dogs [Figure 2]. Decreased mobility of the tongue (n=2), tonsillitis (n=1), and mandibular lymphadenopathy (n=2) also were detected.
Pharyngeal examination under light, general anesthesia initially revealed a soft palate of normal length, but with retraction of the apparent free caudal margin of the soft palate, the soft tissue continued and eventually attached to the caudal pharyngeal wall in all dogs. The excessive tissue could only be seen on elevation or rostral retraction of the edge of the caudal soft palate. The intrapharyngeal ostium between the naso- and oropharynx was only a thin, midline slit (7 to 15 mm long) bordered by thickened, erythematous, and edematous tissues [Figure 3]. Laryngeal function under direct visualization was normal in all dogs.
Diagnostic Imaging
Lateral pharyngeal radiographs were taken in all dogs and revealed similar changes. A thick band of soft tissue (3 to 4 mm wide, 10 to 15 mm long) extended from the terminal soft-palate region to the caudal dorsal laryngopharynx [Figures 4A, 4B, 4C]. No visible communication between the nasopharynx and laryngopharynx could be identified. In some dogs, the whole caudal nasopharynx was obliterated [Figure 4D], either in a neutral lateral view or with bending of the neck. Soft-tissue swelling was seen ventral to the caudal mandible region in three dogs and caudal to the larynx in one dog [Figure 4D].
Thoracic radiographs were taken in all dogs, and an esophageal hiatal hernia was seen in one dog (case no. 3). No evidence of megaesophagus was seen on survey radiographs, but a mild megaesophagus was detected with a barium study.
On swallowing videofluoroscopy (n=6), four dogs had a slightly delayed oral phase, particularly with solid foods. All dogs had varying degrees of pharyngeal dysphagia, in that fluid or food would accumulate in the rostral pharynx and remain there longer than normal. Small parts of the bolus then moved to the cricopharyngeal opening and readily passed caudally, indicating normal cricopharyngeal function in five dogs. The remaining dog had moderate cricopharyngeal dysphagia. Esophageal motility was slightly reduced in four dogs. Tracheal aspiration of barium was seen in all dogs. In one dog, food accumulated in the pharynx, and, when forced caudally by more ingesta, the food would readily pass through the upper esophageal sphincter in small amounts. Immediate regurgitation with repeated swallowing of the regurgitated food was seen in two dogs. Two dogs had successful swallowing movements only when their heads were acutely elevated.
Lingual ultrasonography (n=3) showed that while affected dogs had overall body weights less than the normal dogs, the tongue base averaged 9.8 mm thicker [Table 2; Figure 5]. One dog (case no. 6) that was euthanized for severe dysphagia had the thickest tongue, measuring 13.8 mm more than the tongues of normal dachshunds.
Treatments and Outcomes
Pharyngeal surgery using two surgical procedures was performed in four dogs. In one dog (case no. 1), excess tissues of the palatopharyngeal arch were loosened from their lateral and caudal attachments to the pharyngeal wall. The lateral incisions extended cranially to the caudal margins of the palatine tonsils. The mucosal lining of the intrapharyngeal ostium was excised, and the edges were sutured together. The newly formed soft palate was checked for appropriate length relative to the epiglottis, after which the free edges of the oral and nasal mucosa were sutured together. The surgical defects in the pharyngeal walls also were sutured. The dog improved markedly and was symptom free for 6 months, at which time death occurred from unrelated causes.
Three dogs had similar operations, except that the pharyngeal wall defects were left to heal by secondary intention. In one of these dogs, the tonsils and hyperplastic sublingual mucosa were also removed. These three dogs initially had improved respiratory function with no visible expiratory cheek puff, but these signs recurred after 3 weeks. The dysphagia never improved and continued to worsen postoperatively, especially in the dog (case no. 7) that had a tonsillectomy, and she was euthanized 4 months later. A second dog (case no. 4) was reoperated 10 months later because of worsening of the dyspnea and dysphagia. At the second surgery, a diode laser was used to excise 1 to 2 mm of edematous mucosa from the palatopharyngeal arch; however, the procedure had no beneficial effect, and the dog developed rhinitis shortly after surgery. Marked nasopharyngeal reflux was seen on videofluoroscopy, and a permanent gastrostomy tube was inserted. Four months later the tube was still in place, but the dog was euthanized at the owners’ request. The third dog (case no. 2) was alive 1 year after the surgery, but it had persistent dyspnea and dysphagia.
The two oldest dogs (case nos. 3, 5) had the mildest signs and were treated conservatively except for a hiatal hernia that was repaired. Six of the dogs were fed soft, fine foods from an elevated surface after the diagnosis was made. Case no. 6 was presented with severe dysphagia, macroglossia, and reduced motility of the tongue. The dog was euthanized after the clinical workup, and a postmortem was performed the same day.
Pathological Findings
Tissue removed from two dogs during surgery was sent for histological examination. Microscopic examination showed normal epithelium with prominent edema of the underlying lamina propria. No evidence of inflammation or other anomalies was found.
A detailed anatomical dissection of the head and neck was done at the time of postmortem of case no. 6. The skin was carefully dissected from the underlying muscle, which was then exposed in layers in order to examine each muscle and the associated neurovascular structures. Macroscopically, the mylohyoid muscle in the submandibular triangle was normal, but both the geniohyoid and genioglossus muscles were hypertrophic and firm. The neck muscles were normal and were dissected until the trachea and larynx were exposed. The caudal pharyngeal wall, epiglottis, and caudally extending soft palate with its slit-like opening to the nasopharynx were exposed [Figures 6, 7]. The palatopharyngeal arch was thickened and edematous. On opening the soft palate, the mucosa of the nasopharynx was erythematous and edematous, with prominent lymphoid hyperplasia of the nasopharyngeal wall. Microscopic examination of the palatopharyngeal arch showed normal skeletal muscle bundles of varying thickness within the palatopharyngeus muscle. Prominent lymphoid hyperplasia and reactive follicular hyperplasia were seen in the sections taken from the nasopharyngeal wall and mandibular lymph nodes, but they were considered nonspecific. No other postmortem abnormalities were found.
Discussion
Embryological development of the palate starts around the third week of gestation. Two lateral palatal shelves originate from the maxillary processes of the first pharyngeal arch to form the secondary palate.13 Initially the palatal shelves are vertically oriented alongside the developing tongue, but eventually they elevate and fuse in the midline. They also fuse with the nasal septum dorsally and the primary palate rostrally to form the hard and soft palates.13 The muscles of the soft palate develop from the caudal third of the lateral palatine processes and consist of the paired mm. palatine, tensor veli palatini, levator veli palatini, pterygopharyngeus, and palatopharyngeus.13,14
The study reported here describes an unusual nasopharyngeal stenosis seen in smooth-haired dachshunds over a 3-year period. Besides a prior case report by one of the authors, nasopharyngeal stenosis has not been reported in dachshunds and has not been documented in the caudal nasopharynx.12
In the affected dachshunds, the palatopharyngeal arch extended caudally to attach to the lateral and caudal pharyngeal walls, meeting each other in the midline. On dissection, hypertrophic and abnormally long palatopharyngeus muscles seemed to be the muscles responsible for the nasopharyngeal stenosis and narrowed nasopharyngeal ostium. The palatopharyngeus muscles normally originate from the palatine aponeurosis and extend laterally and dorsally in the pharynx to form the base of the palatopharyngeal arches.14
The exact developmental pathophysiology of this disorder is still unclear, but the authors believe the condition originates as a primary palatopharyngeal dysgenesis. The resulting slit-like defect may act as a one-way valve allowing inspired nasal air to reach the larynx but blocking the passage of expired air during expiration. Some expired air subsequently passes out through the mouth. Dorsal displacement of the abnormal membrane with possible temporary obliteration of the caudal nasopharynx may also occur during expiration. As the condition progresses and secondary edema and inflammation develop, the slit may become even smaller, thereby accentuating the clinical signs. The affected dogs had no conscious open-mouth breathing; hence, the very characteristic cheek puff was seen. The owners were often unaware of this cheek puffing or believed it to be normal.
Dysphagia may be oral, pharyngeal, cricopharyngeal, or esophageal in origin; or it may arise from a combination of these.15,16 Causes include functional motor disorders of the central and peripheral nervous system, neoplasia, foreign bodies, trauma, and structural masses.15,16 The dogs in this study all had pharyngeal dysphagia, and one dog had additional cricopharyngeal dysphagia. Some dogs also showed slight oral phase abnormalities. In order for a food bolus to move caudally from the base of the tongue, it must be pushed caudodorsally—the so-called plunger action.15 Additionally, active palatopharyngeal and caudal pharyngeal wall contraction and cranial movement of the larynx and cricopharyngeal area are required.15 In these dogs, macroglossia seemed to cause poor lingual plunger action, and the excessive palatopharyngeal tissues may also hamper pharyngeal contractions. Only when the bolus of food reached the cricopharyngeal area was swallowing usually initiated. In affected dogs, soft foods were handled much better than dry foods, as has been described with other pharyngeal dysphagias.15
Six of the dogs were presented with macroglossia, and it was so severe in one dog that he was euthanized after presentation. It was unclear whether the macroglossia arose from primary hyperplasia of the affected glossal muscles, in association with the hyperplastic palatopharyngeus muscles, as an embryologic developmental disorder; from muscular hypertrophy secondary to the palatopharyngeal abnormality; or from a combination of these. The extrinsic tongue muscles play a critical role in the oral phase of swallowing.14 The digastric, mylohyoid, and geniohyoid muscles facilitate tongue movement and slight elevation of the hyoid.17 Fluoroscopic studies in the affected dogs indicated that lingual hypertrophy secondary to the nasopharyngeal stenosis was unlikely or only a minor contributing factor, because the caudodorsal pharyngeal structures appeared to function normally. The macroglossia was postulated as the primary cause of the dysphagia, and the nasopharyngeal stenosis seemed to play a lesser role.
Surgical intervention improved the condition of one dog, but improvement in three other dogs lasted only a few weeks before clinical signs returned. From this limited study, no recommendations can be made regarding which specific surgical technique is best. Care should be taken, however, to not remove too much palatal tissue, as this might lead to nasopharyngeal reflux and secondary rhinitis. Suturing of the pharyngeal wall defects was only done in the one case that did well postoperatively. Dogs with marked macroglossia have a poor prognosis, and surgery may be contraindicated.
The presence of a hiatal hernia in one dog of this study, as well as in a previously reported case, was unexpected.12 In the previously reported case, the hiatal hernia resolved after pharyngeal surgery relieved the respiratory effort.12 In one study, bulldogs with nontraumatic hiatal hernias also had severe respiratory efforts associated with brachiocephalic syndrome.18 It may be wise to perform pharyngeal surgery before hiatal hernia repair, as the latter may then resolve on its own. Also, any dog presented with an incidental finding of hiatal hernia should raise suspicions of an accompanying pharyngeal problem.
As no pedigree analysis could be obtained, a hereditary component cannot be excluded at this stage.
Conclusion
Nasopharyngeal dysgenesis was diagnosed in seven dachshunds and was characterized by expiratory cheek puffing, upper respiratory dyspnea, and dysphagia. Nasopharyngeal stenosis was confirmed by lateral pharyngeal radiographs and direct visualization of the nasopharynx. A transmandibular finger test and lingual ultrasonography were reliable, noninvasive indicators of macroglossia. The exact pathogenesis is still speculative, and genetic studies are warranted to elucidate possible hereditary factors and to prevent propagation of this condition.
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Citation: Journal of the American Animal Hospital Association 42, 4; 10.5326/0420290
Transmandibular finger test in a normal dachshund. The index finger is placed transversely under the mandible at the level of the lip commissure and pressed against the ventral rami. No soft tissues in the intermandibular space prevent the finger from contacting the rami.
An affected, 2.5-year-old, male dachshund (case no. 4) in dorsal recumbency under general anesthesia. The intermandibular soft tissues (black arrows) extend beyond the ventral borders (white arrows) of the mandible at the level of the lip commissure. A finger placed across the chin in this area would not touch the rami of the mandibles.
Intraoral view of the nasopharynx of a 2-year-old, male dachshund (case no. 1), revealing a slit-like intrapharyngeal ostium (black arrow). Note the ridge of the caudal soft palate that separates the soft palate from the abnormal soft tissue (white arrows). An endotracheal tube (asterisk) is visible ventrally, and an enlarged tonsil is visible to the left, just medial to the dental arcade.
(A) Lateral pharyngeal radiograph of a normal dachshund. Note the epiglottis (arrow) caudal to the termination of the tip of the soft palate (arrowheads) and the radiolucent gap between the nasopharynx and the entrance to the larynx. (B) Lateral pharyngeal radiograph of a mildly affected, 4-year-old, female dachshund (case no. 2) under general anesthesia. Arrowheads indicate a membrane separating the nasopharynx from the laryngopharynx. (C) Lateral pharyngeal radiograph of a moderately affected, 2-year-old, male dachshund (case no. 1). Arrowheads indicate a membrane separating the nasopharynx from the laryngopharynx. (D) Lateral pharyngeal radiograph of a severely affected, 2.5-year-old, male dachshund (case no. 4) with poor long-term response to surgery. Note the totally obliterated caudal nasopharyngeal region (***) and the submandibular (arrowheads) and ventral cervical (+++) soft-tissue swellings secondary to hypertrophy of the muscles. The slight neck flexion did not contribute significantly to these abnormalities.
Ventral sagittal intermandibular ultrasonogram of the base of the tongue, made with a 7.5-MHz linear array transducer in a severely affected, 1-year-old, male dachshund (case no. 6). The tongue has a thickness of 31 mm (distance between the arrows).
Postmortem photograph of the ventral aspect of the pharyngeal area of case no. 6 after splitting the mandible and tongue. Note the excessive soft tissue and the slit-like intrapharyngeal ostium (also see Figure 7), which appears more oval in shape because of lateral traction of the split structures. The upper dental arcade and hard palate are visible at the top of the figure.
