Brachycephalic airway obstructive syndrome is characterized by any combination of stenotic nares, elongated soft palate, and everted laryngeal saccules.[1-6] Some authors consider laryngeal collapse as a component of brachycephalic syndrome,[1, 7] and in the Bulldog, tracheal hypoplasia also can be found. Nasal narrowing and tracheal hypoplasia are considered as primary abnormalities, eversion of the saccules and laryngeal collapse are attributed to upper airway obstruction, and elongated soft palate generally is a primary condition, but it could possibly become elongated or thickened because of negative inspiratory pressure within the airway, a process that occurs in other pharyngeal tissue.[7, 8] Nasopharyngeal turbinates also can contribute to upper airway obstruction, are found most often in Pugs, and are likely a primary or congenital abnormality associated with shortening of the muzzle.
The brachycephalic phenotype is defined by a severely shortened muzzle in a short and wide head; prognathism and wide-set prominent eyes are common. Quantification of brachycephaly is performed by calculating the skull index of the head. Subjects with a skull width-to-length ratio >0.8 are categorized as brachycephalic. In contrast, mesocephalic dogs have a smaller width-to-length ratio.[10, 11] Typical breeds affected by bracycephalic syndrome include the English and French Bulldog, Pug, Boston Terrier, and Shi Tzu, and the chromosomal location for brachycephaly recently has been identified on Cfa 1 using genome-wide association. The Norwich Terrier does not phenotypically resemble breeds with brachycephalic syndrome, but owners and breeders of Norwich Terriers have expressed concern regarding respiratory difficulty in the breed, and the Norwich and Norfolk Terrier Club (USA) has formed a “Health and Genetics Sub-Committee for Research on Upper Airway Syndrome in Norwich Terriers”.1 Genetic analysis of affected and unaffected dogs is ongoing as is investigation into the role of skull shape in brachycephaly.[12, 13]
Specific examination findings and typical phenotypic appearance allow early recognition of brachycephalic syndrome, and surgical therapies such as stenotic nares resection, staphylectomy, and sacculectomy are associated with excellent outcome in most cases.[2, 3, 5, 6] The purpose of this study was to describe signalment, historical data, clinical findings, laryngoscopic appearance, therapeutic interventions, and response to treatment in 16 Norwich Terriers examined by a single clinician (L.R.J.).
Materials and Methods
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- Materials and Methods
Norwich Terriers presented to the University of California, Davis William R. Pritchard Veterinary Medical Teaching Hospital (UCD VMTH) for examination of the upper respiratory tract between February 2010 and March 2013 were prospectively evaluated. The electronic medical record system also was searched for all additional Norwich Terriers presented during this time frame. Specific data collected for study dogs included age, sex, body weight, and body condition score at the time of initial examination. A complete respiratory history including any previous airway examinations or surgeries was recorded. All dogs included in this study received standard physical and laryngoscopic examinations performed by one of the authors (L.R.J.). Physical examination included subjective assessment of size of the external nares, evaluation of nasal airflow, soft palate palpation, and auscultation of the larynx, trachea, and lungs as well as a general physical examination.
Anesthetic protocols were individualized for each dog as determined by members of the UCD VMTH Anesthesia Service. Laryngoscopy was performed in all dogs using a rigid or flexible endoscope,2,3 and was digitally recorded for future review. Oropharyngeal features assessed during laryngoscopy included tonsils, soft palate length, laryngeal saccules, laryngeal structure, and laryngeal function. Specifically, tonsils were examined for enlargement, hyperemia, and position (in or out of crypts). Soft palate length was assessed in relation to the caudal tonsillar crypts and the degree of overlap of the epiglottis (in mm) was estimated. The larynx was assessed for edema or hyperemia, and the size and position of the arytenoids was noted. The internal opening of the larynx was subjectively assessed for size and conformation. Degree of laryngeal collapse was graded using the classification scheme described by Leonard, with saccular eversion classified as Grade 1 and collapse involving the cuneiform or corniculate processes of the arytenoids as Grade 2 or 3, respectively. Laryngeal function was considered appropriate if abduction was noted on inspiration under a light plane of anesthesia with or without stimulation of respiration with doxapram hydrochloride. Results of endoscopy were summarized and digital files were reviewed for consistency in reporting.
When clinically indicated, endoscopic examination of the choanae, trachea, and bronchi was performed after laryngoscopic examination. The choanae were evaluated for symmetry and size by use of a flexible endoscope3 in a retroflexed position above the soft palate. The trachea was examined using a rigid2 or flexible3 endoscope. Tracheal collapse was identified and characterized based on the grading scheme of Tangner and Hobson.
Depending on presenting complaints and clinical findings, cervical and thoracic radiography or computed tomography of the skull sometimes were performed. Radiographs were performed in awake animals and images were reviewed by a board-certified radiologist (A.H.C.) who was blinded to the clinical presentation of the dogs. Computed tomographic4 studies were performed with the dogs in sternal recumbency and under general anesthesia. Images were obtained using bone and soft tissue algorithms with reformatted 0.6 mm images of the area of interest. A single observer (A.H.C.) retrieved DICOM CT images for each dog and reviewed them on a dedicated image viewing station using commercially available viewing and analysis software.5 Transverse images were used primarily for evaluation, but sagittal and dorsal multiplanar reformatting images also were used at the viewer's discretion. In dogs that had skull CT performed, skull index was calculated as the width-to-length ratio of the skull as described.
Medical and surgical interventions were retrieved from the medical record. Response to the treatment was determined by follow-up examination or telephone conversations with owners. Owners provided a subjective assessment of overall health, activity level, breathing pattern (normal or labored), respiratory sounds (quiet or noisy/loud), and indicated current medications being used. All physical examinations and telephone interviews were conducted by the same author (L.R.J.).
Age, weight, and body condition score were assessed for normality using D'Agostino & Pearson omnibus normality test.6 Normally distributed data are presented as mean ± standard deviation; non-normally distributed are presented as median with range.
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- Materials and Methods
Brachycephalic obstructive airway syndrome is a serious and life-threatening condition that requires identification and intervention to avoid asphyxiation, particularly during anesthetic induction or recovery. This study identified several features in Norwich Terriers similar to brachycephalic airway disease and reports new findings in obstructive upper airway disease. Firstly and most importantly, approximately 1/4 of Norwich Terriers in this study were presented for airway screening in the absence of clinical complaints of respiratory disease. Without owner or breeder awareness of the type of abnormalities found in this breed, the condition would have gone undiagnosed. In the dogs examined here, supra-arytenoid swelling and laryngeal narrowing necessitated use of an endotracheal tube smaller than would be used in a dog of comparable weight. This highlights the fact that Norwich Terriers should be considered challenging anesthetic candidates similar to classic brachycephalic breed dogs and should be watched carefully in postanesthetic recovery because of the potential for airway obstruction.
Secondly, half of the Norwich Terriers examined here had normal physical examination findings, despite subsequent identification of severe airway obstruction. This finding may have been impacted by clinical bias because the examiner was not masked to the presence or absence of clinical signs. However, knowledge of the clinical presentation should have led to increased awareness of abnormal respiratory noise and overinterpretation of respiratory sounds, rather than normal physical examination findings. Typical findings in classic brachycephalic dogs include a combination of elongated soft palate, stenotic nares, and everted laryngeal saccules,[3, 5] although some dogs have only 1 or 2 components of the syndrome. Given the lack of clinical signs, lack of external evidence of brachycephalic syndrome, and a normal physical examination, laryngoscopic examination is essential to determine the presence or absence of obstructive laryngeal disease in Norwich Terriers. Appropriate screening of breeding animals by an experienced observer will be essential to decrease the occurrence of this syndrome in the breed.
In typical brachycephalic breeds, an association between stenotic nares, everted laryngeal saccules, and everted tonsils is reported, suggesting that nasal obstruction with associated alterations in air flow causes microtrauma and secondary changes to soft tissue structures. However, in the Cavalier King Charles Spaniel, external nasal structures typically are normal, with elongated soft palate and laryngeal collapse found most commonly, suggesting an alternate site of airflow obstruction in this breed. In the group of Norwich Terriers examined here, no nasal obstruction was noted and the palate was normal in most dogs. The site of obstruction appeared to be at or within the larynx, with narrowing caudal to the vocal fold that decreased luminal diameter, presumably leading to airflow obstruction, trauma to upstream tissues, and severe redundancy of supra-arytenoid tissue that further obstructed air flow.
Redundant supra-arytenoid tissue has been reported with congenital laryngomalacia, a disorder of uncertain etiology in humans.[15-17] Laryngeal collapse is recognized as a component of brachycephalic syndrome and also has been reported in very young (<6 months old) brachycephalic dogs. Additional investigations are needed to determine if congenital laryngomalacia affects dogs and whether the condition described in Norwich Terriers examined represents a variant of this syndrome. Most dogs in this study were young when clinical signs prompted veterinary care, but some dogs appear to have compensated well for the syndrome, presenting for evaluation as late as 6 and 11 years. Redundant supraglottic tissue also has been reported in a human patient with acquired laryngeal dysfunction associated with previous trauma, and it is plausible that supra-arytenoid swelling in the Norwich Terriers examined here developed secondary to airflow obstruction at the level of the larynx. Subsequent laryngeal collapse may have resulted from mechanical compression of cartilage by swollen supra-arytenoid tissue or by interference with muscular abduction of the cartilage. Interestingly, this tissue swelling has not been reported previously in dogs with laryngeal collapse or laryngeal paralysis, suggesting something distinct about the Norwich Terrier breed. Also, the swelling and laryngeal collapse resolved in 1 dog that had bilateral sacculectomy performed here, suggesting that partial alleviation of airway obstruction was sufficient to decrease trauma to tissue and swelling of tissue folds, although persistent or recurrent clinical signs in the remaining dogs treated in similar fashion suggests that such resolution is uncommon.
The role of surgery in the airway syndrome of Norwich Terriers is unclear. Resection of stenotic nares and staphylectomy are well-established techniques for brachycephalic breeds with excellent outcome reported when the procedures are performed by experienced surgeons.[2, 5, 18] Sacculectomy remains a controversial surgical technique in brachycephalic syndrome because eversion is a secondary process, and it has been suggested that eversion will resolve when obstruction to airflow is alleviated by other surgical procedures. However, this theory was refuted by a previous study in which staphylectomy, nares resection, and unilateral saccular resection failed to result in regression of contralateral saccular swelling. Interestingly, our study documented return of mucosal eversion post-resection of the saccules, which could result in recurrence of obstruction to airflow. Surgeons should take care to remove as much everted saccular tissue as feasible and relieve the upper airway obstruction as effectively as possible to avoid this late sequela. Clients also should be warned that if the primary anatomical abnormalities cannot be completely resolved, saccule eversion can recur. Repeat airway examination should be performed if respiratory obstruction recurs.
Computed tomography in 2 dogs examined here suggested narrowing in the ventral region of the thyroid cartilage in the position that also appeared narrowed during laryngoscopy, although CT was performed under anesthesia with endotracheal intubation. Three dimensional reconstruction of CT images has proved valuable in identifying specific causes of laryngeal and tracheal obstruction in dogs, but to the authors' knowledge, no information is available on laryngeal dimensions in small breed dogs or in brachycephalic dogs that could be compared to findings in the Norwich Terriers of this study. Further investigation is required, along with physiologic and anatomic assessment.
Airway obstructive disorders can be life threatening and in the absence of obvious physical examination features of brachycephalic syndrome, additional means are needed to identify affected dogs. Barometric whole body plethysmography has been used to identify functional parameters that distinguish between normal and brachycephalic breeds. Expiratory-to-inspiratory time ratio is close to 2.0 in normal dogs and is decreased in brachycephalic dogs consistent with obstruction to inspiratory flow. Peak expiratory-to-inspiratory flow ratio is higher in brachycephalic dogs than in normal dogs as a reflection of extrathoracic obstruction to inspiratory airflow. Unfortunately, pulmonary function testing is not readily available in veterinary medicine, but this would be a useful noninvasive screening tool. Recently, biomarkers have been assessed in dogs with brachyphalic syndrome, and approximately half of affected dogs showed increased cardiac troponin concentrations. However, this may be more important as a marker of cardiac strain in brachycephalic dogs than as a marker of respiratory disease. Evidence of systemic inflammation also has been discovered in brachycephalic dogs, with significantly higher plasma concentrations of inflammatory cytokines TNF-α, IL-10, IL-13, and IL-17A as well as increased nitrated proteins compared to control dogs. It is unclear whether any of these markers could be used within a breed to distinguish normal from affected dogs.
Specific genetic analysis has not been performed in breeds such as the Norwich Terrier and Cavalier King Charles Spaniel that display only selected features of brachycephalic syndrome, but findings of breed distinctions in the manifestation of brachycephalic syndrome suggest that variable genes or differential expression of genes involved in brachycephaly could be involved in various dog breeds. Increased awareness of brachycephalic features in atypical breeds is important for providing a safe anesthetic episode. Further investigation and selective breeding away from affected individuals will be important for the survival and success of the Norwich Terrier breed.