Abstract
OBJECTIVE To assess feasibility of flexible endoscopic evaluation of swallowing (FEES) in awake dogs, determine whether specific variables associated with the oropharyngeal phase of swallowing can be recognized, and evaluate the safety and tolerability of FEES.
ANIMALS 6 healthy client-owned large- and giant-breed adult dogs.
PROCEDURES A topical anesthetic was applied to the nasal passage of each dog, and a fiberoptic endoscope was passed transnasally until the tip of the scope was positioned in the oropharynx. All dogs voluntarily drank colored water followed by consumption of a commercial canned diet and then a kibble diet mixed with food color. During each swallow, laryngeal and pharyngeal anatomic structures were evaluated and depth of bolus flow prior to the pharyngeal phase of swallowing was assessed. Evidence of bolus retention in the vallecula or pyriform sinuses and laryngeal penetration of the bolus were recorded.
RESULTS FEES was completed without major adverse events and was tolerated well by all 6 dogs. Mild, self-limiting epistaxis was noted for 2 dogs. The nasopharynx, oropharynx, and hypopharynx were observed in all dogs; movement of food boluses through the esophagus was observed in 2 dogs, and food boluses in the stomach were visible in 1 dog. Pharyngeal and laryngeal function was considered physiologically normal in all dogs.
CONCLUSIONS AND CLINICAL RELEVANCE FEES appeared to be a feasible diagnostic tool for use in large- and giant-breed dogs. Studies are warranted in dogs with oropharyngeal dysphagia to determine whether FEES can be tolerated and whether it can augment videofluoroscopy findings.
Dysphagia is a relatively common disorder in dogs and can result from an abnormality in the oral, pharyngeal, pharyngoesophageal, or esophageal phase of swallowing.1 Oropharyngeal dysphagia affecting the pharyngeal or pharyngoesophageal phases of swallowing can be challenging to diagnose and is characterized by abnormal bolus transport from the oropharynx to the hypopharynx or from the hypopharynx to the esophagus.2–4 Dogs with oropharyngeal dysphagia often have nonspecific signs such as gagging, retching, coughing, nasal reflux, dehydration, malnutrition, aspiration pneumonia, and repeated swallowing attempts prior to the successful movement of a bolus into the proximal portion of the esophagus.4,5 The ability to evaluate pharyngeal function is important because pharyngeal dysfunction is an important predictor for aspiration in humans6 and can occur secondary to cricopharyngeus muscle dysfunction.7
Standard diagnostic evaluation of most dysphagic dogs involves a combination of historical information, results of comprehensive physical and neurologic examinations, observation of the animal during eating and drinking, assessment of survey radiographs of the cervical region and thorax, and videofluoroscopic assessment of swallowing.3,5 Survey radiography and static radiographic assessment of barium swallowing are frequently of limited diagnostic value because many of the disorders associated with oropharyngeal dysphagia do not substantially alter the anatomy but instead result in abnormal function. Dynamic contrast studies conducted by use of videofluoroscopic surveillance or direct visual examination of the oropharynx with endoscopy are necessary to accurately diagnose an abnormality. Videofluoroscopy allows determination and timing of the sequence of events that comprise a swallow.2,8 Additionally, the movement of certain anatomic structures is measured in relation to a fixed point to allow further assessment of function.8
The FEES is an instrumental assessment of deglutitive function that involves use of a flexible endoscope passed transnasally in awake human patients to allow visual examination of pharyngeal and laryngeal structures during swallowing.9 Equipment for the FEES procedure is portable and can easily be moved to a bedside or other location for patient examination. Food and liquid boluses are consumed by patients during the procedure so that clinicians can view structural movements of the pharynx and larynx, bolus transit, and airway protection.9
To our knowledge, the feasibility and application of FEES have not been evaluated in awake nonsedated dogs. Thus, the objective of the study reported here was to determine whether specific variables associated with the oropharyngeal phase of swallowing could be recognized via FEES in healthy awake dogs and to evaluate the safety and tolerability of FEES.
Materials and Methods
Animals
Six healthy client-owned large- or giant-breed adult dogs (2 Golden Retrievers, 1 English Springer Spaniel, 1 Labrador Retriever cross, 1 Bull Mastiff cross, and 1 Great Pyrenees cross; 5 castrated males and 1 spayed female) were enrolled in the study. Dogs ranged from 1 to 11 years of age (mean, 5.5 years; median, 6 years). Body weight ranged from 24.7 to 36.0 kg (mean, 32.4 kg; median, 33.0 kg). Body condition score (scale, 1 to 9) ranged from 4.0 to 5.5 (mean, 4.8; median, 5.0). All dogs included in the study had no history of gastrointestinal tract disease within the past 12 months and no history of dysphagia. A comprehensive physical examination was performed on all dogs, and blood samples were collected for a CBC, serum biochemical analysis, and measurement of creatinine kinase activity. The study was approved by the Institutional Animal Care and Use Committee at the University of California-Davis School of Veterinary Medicine, and client consent was obtained from owners prior to enrollment of dogs in the study.
Procedures
Food was withheld from all dogs overnight. The following morning, each dog was carefully restrained in a sitting position on an examination table by 2 or 3 animal health technicians. A fiberoptic endoscopea with an outer shaft diameter of 2.9 mm, tip diameter of 2.5 mm, and length of 100 cm was used for all dogs. The right nasal passage was anesthetized with 4 or 5 drops of topical anesthetic.b The tip of the endoscope was lubricated with sterile lubricating gelc and then inserted into the ventral meatus of the nasal passage. The nasal philtrum was pushed dorsally by the thumb of the investigator to facilitate passage of the endoscope into the ventral meatus. The endoscope was advanced until the tip of the scope was positioned between the soft palate and the tip of the epiglottis; at this location, the base of the tongue, vallecula, larynx, and both pyriform sinuses were visible. Dogs voluntarily drank 20 mL of water mixed with 2 drops of green food color,d and 8 to 10 swallows were closely observed and recorded on a video capture unit.e Dogs then were offered boluses of a commercial canned diet formulationf (5 to 7 g/bolus) mixed with green food color (6 drops of food color/0.25 can) to help discern food and liquid boluses from the surrounding mucosa. Finally, dogs were offered boluses of a commercial kibble formulationg (3 kibbles/bolus). Eight to 10 swallows were closely observed and recorded for each food type.
During each swallow, laryngeal and pharyngeal anatomy was evaluated to determine integrity of the pharyngeal phase of the swallow. This examination provided information about the ability to protect the airway during swallowing, ability to initiate a swallow without spillage of material into the hypopharynx, timing and direction of movement of the bolus through the hypopharynx, ability to completely clear the bolus from the pharynx into the esophagus during the swallow, and presence of pooled or residual material in the hypopharynx. Specific abnormalities involving integrity of pharyngeal function that were evaluated included depth of bolus flow to at least the vallecula prior to the pharyngeal phase of the swallow, evidence of bolus retention in the vallecula or pyriform sinuses after the pharyngeal phase of the swallow, laryngeal penetration (defined as the presence of bolus material within the laryngeal vestibule that does not pass below the level of the vocal folds before or after the pharyngeal phase of the swallow), and tracheal aspiration (defined as bolus material below the level of the vocal folds before or after the pharyngeal phase of the swallow). In addition, an attempt was made to endoscopically monitor movement of the food bolus from the hypopharynx into the distal portion of the esophagus in 2 dogs and into the stomach in 1 of these 2 dogs. This systematic evaluation allowed investigators to observe and record typical movement, timeliness, and laryngeal penetration in these 6 clinically normal dogs.
The ease of endoscopic placement in the nasopharynx was graded on a scale of 1 to 5 (1 represented easy placement with no or minimal resistance by the dog and only a single attempt required for successful endoscopic placement, and 5 represented difficult placement because of a lack of compliance by the dog, the need for an additional technician to provide restraint, and ≥ 5 attempts for successful endoscopic placement; Appendix 1). In addition, tolerance of dogs to the FEES procedure was also graded on a scale of 1 to 5 (1 reflected that the procedure was tolerated well and the dog required minimal restraint and offered minimal resistance after placement of the endoscope in the nasopharynx, and 5 reflected that the procedure was poorly tolerated with severe resistance by the dog [characterized as repeated head shaking, sneezing, and attempting to stand after placement of the endoscope in the nasopharynx] and an additional technician was needed to help restrain the dog and keep it in a sitting position; Appendix 2).
Results
The FEES procedure was successfully completed in all 6 dogs, although the ease of endoscopic placement and tolerance of the procedure differed among dogs. The FEES procedure required < 25 minutes to complete in all dogs, and video of the procedure was recorded for all dogs.
The most challenging aspect of the procedure was initial placement of the endoscope in the nasopharynx, with scores for ease of endoscopic placement ranging from 1 to 4 (mean ± SD, 2.5 ± 1.4; median, 2.5). Overall, the procedure was tolerated well, with tolerance scores ranging from 1 to 3 (mean ± SD, 1.5 ± 0.8; median, 1.0). None of the dogs aspirated during the procedure. One dog (English Springer Spaniel) had multiple sneezing episodes after placement of the endoscope; however, restraint of the dog's head during the sneezing episodes prevented dislodgment of the endoscope. In addition, mild self-limiting epistaxis was observed in 2 dogs (Labrador Retriever cross and Great Pyrenees cross), but it resolved without treatment within 2 minutes for both dogs.
Results of evaluation of the pharyngeal region and larynx were unremarkable for all dogs (Figures 1–3). The nasopharynx, oropharynx, and hypopharynx (including the pyriform fossa, epiglottis, aryepiglottic fold, and cricoid cartilage) were visible in all dogs. No dogs had evidence of bolus retention in the hypophartracheaynx. Laryngeal structure and function could be evaluated in all dogs and was deemed to be physiologically normal for all dogs. Silent aspiration owing to spillage of the bolus into the laryngeal vestibule, glottis, and was not observed before a swallow in any dogs. Furthermore, no dogs had retention of the bolus in the vallecula (Figure 4), pyriform sinuses (Figure 5), and laryngeal vestibule after a swallow. Several boluses of kibble were visible as they moved through the esophagus (Figure 6) and lower esophageal sphincter of 2 dogs, and food boluses were visible as they entered the stomach of 1 of these dogs.
Endoscopic image of the larynx of a representative dog before bolus administration. Notice the right aryepiglottic fold (arrows), arytenoids (A), and vocal folds (arrowheads).
Citation: American Journal of Veterinary Research 77, 3; 10.2460/ajvr.77.3.294
Endoscopic image of the epiglottis of a representative dog during bolus passage. The whiteout phenomenon is attributable to retroflection from the epiglottis during this phase of swallowing.
Citation: American Journal of Veterinary Research 77, 3; 10.2460/ajvr.77.3.294
Endoscopic image of the tip of the epiglottis (E) of a representative dog during passage of a bolus of canned food into the hypopharynx.
Citation: American Journal of Veterinary Research 77, 3; 10.2460/ajvr.77.3.294
Endoscopic image of the wedge-shaped space representing the vallecula (arrows) between the base of the tongue and epiglottis in a representative dog. E = Tip of the epiglottis.
Citation: American Journal of Veterinary Research 77, 3; 10.2460/ajvr.77.3.294
Endoscopic image of the funnel-shaped pyriform sinuses (P) in a representative dog. The pyriform sinuses are bounded laterally by the hypopharyngeal wall and medially by the aryepiglottic fold. E = Laryngeal surface of epiglottis. VF = Vocal fold.
Citation: American Journal of Veterinary Research 77, 3; 10.2460/ajvr.77.3.294
Endoscopic images of the esophagus of a representative dog during swallowing. A—Collapsed midesophageal lumen prior to passage of a liquid bolus. B—Distended esophagus as the leading edge of a liquid bolus is about to enter it. C—Passage of a liquid bolus ahead of a peristaltic wave. D—Esophageal lumen after passage of a liquid bolus.
Citation: American Journal of Veterinary Research 77, 3; 10.2460/ajvr.77.3.294
Discussion
In the study reported here, feasibility for the use of FEES in nonanesthetized dogs was evaluated. The procedure was well tolerated by all dogs; mild self-limiting epistaxis in 2 dogs was the only complication observed. Epistaxis is the most common complication reported with FEES in humans, and it occurs in < 1% of patients.10 Laryngospasm is the most serious complication with FEES that can occur during vigorous manipulations of the vocal cords in humans,10 but laryngospasm was not evident in the dogs of the present study.
All dogs readily accepted boluses of the canned and kibble formulations during FEES, and the procedure facilitated observation and dynamic assessment of the nasopharynx, oropharynx, and hypopharynx (including the pyriform fossa, epiglottis, aryepiglottic fold, and cricoid cartilage; Figures 1–3). The esophagus was successfully observed during swallowing in 2 dogs during which a bolus was monitored as it moved through the esophagus and lower esophageal sphincter (Figure 4). This may provide a novel method for assessment of functional esophageal motility for clinicians and researchers who lack access to videofluoroscopy. In addition, the procedure allowed us to evaluate the stomach of 1 dog.
Transnasal laryngoscopy has been used to assess laryngeal structure and function in awake and sedated horses and cattle for many years.11–14 Diagnostic utility of transnasal laryngoscopy versus transoral laryngoscopy for evaluation of laryngeal structure and function in dogs with laryngeal paralysis has been evaluated.15,16 However, dogs in both of those reports15,16 were sedated with an opioid analgesic and acepromazine administered parenterally before the start of the procedure. In one of those reports,15 6 dogs were mildly to moderately sedated after administration of the premedications, and 1 dog was severely sedated and could not actively lift its head or resist initial manipulations, which potentially altered laryngeal and pharyngeal function in those dogs. Opioids can induce profound effects on the respiratory system in all species.17 It was suggested by the authors of 1 study18 that acepromazine enhances the negative effects of opioids and other induction agents on laryngeal function. In an aforementioned study,15 one of the control dogs that received the highest dose of acepromazine had diminished laryngeal motion during examination, which underscored the negative effects of sedatives and anesthetics on laryngeal function. Objective evaluation of anatomic structures involved with the swallowing reflex was not performed in studies15,16 conducted to evaluate the use of transnasal laryngoscopy for assessment of laryngeal function in dogs, and no food or water was given to those dogs during the procedures.
Disorders (pharyngeal weakness, cricopharyngeal achalasia, and asynchrony) affecting the integrity of the pharyngeal phase of swallowing and assessment of pharyngeal esophageal anatomy during swallowing in dogs is typically assessed via observation of an animal during eating and drinking, which is followed by survey radiographs of the thorax and cervical region and videofluoroscopic examination during swallowing of liquid barium and barium-soaked food.5 Fiberoptic endoscopic evaluation of swallowing in humans has been compared with videofluoroscopy to discern whether FEES yields important swallowing findings relative to delay in swallowing initiation, laryngeal penetration, and aspiration and pharyngeal residue. Reports19–21,h have indicated that FEES is as sensitive as or more sensitive than videofluoroscopy for assessment of these 4 swallowing variables. The specific advantages for an FEES examination versus videofluoroscopy for evaluation of swallowing in humans have been elucidated and include being able to perform the examination at a bedside location for bedridden, medically unstable, or weak patients and being able to examine patients for which there is a concern about excess radiation exposure.22 In addition, FEES is more sensitive than simple observation of a patient during eating or drinking because the depth and severity of laryngeal penetration can be precisely assessed and retention of a bolus in the vallecula or pyriform sinuses after a swallow can be recognized.19 Tracheal aspiration below the level of the vocal folds before or after the pharyngeal phase of swallowing does not necessarily induce a cough reflex, and FEES is essential to diagnose such silent aspiration.23
In humans, FEES is a valuable tool for use in determining conditions that a dysphagic patient can tolerate for various oral consistencies without undue risk for aspiration and in sufficient quantity to meet caloric needs.22 It is rare for people who are evaluated for dysphagia to need both videofluoroscopy and FEES, although whenever a problem is not fully explained by the results of one procedure, then the other procedure should be performed.
The size of the endoscope used in the study reported here may limit its use in smaller awake dogs. The dogs in the present study all had a body weight > 24 kg, and assistance provided by 3 animal health technicians was needed to adequately restrain the dogs in a sitting position while the endoscopist performed the procedure. The authors have successfully passed an 8F (2.75 mm) esophageal manometry probe transnasally in anesthetized dogs that weighed 5 kg; however, the procedure would be more challenging to perform in awake dogs.
In the study reported here, FEES was well tolerated by healthy awake large- or giant-breed dogs. The FEES examination facilitated comprehensive evaluation of the pharyngeal phase of swallowing and anatomic assessment of the larynx and pharynx in all dogs, movement of the food boluses through the esophagus in 2 dogs, and movement of food boluses into the stomach of 1 dog. Further studies are warranted to compare the diagnostic use of videofluoroscopy versus FEES in healthy dogs and to evaluate the feasibility for use of FEES in dysphagic dogs with oropharyngeal disease, dyspneic dogs with laryngeal paralysis, and dogs with suspected esophageal dysmotility.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| FEES | Flexible endoscopic evaluation of swallowing |
Footnotes
Model 60003VB, Karl Storz Imaging Inc, Goleta, Calif.
Tetracaine HCl ophthalmic solution (0.5%) USP, Bausch & Lomb Pharmaceuticals Inc, Tampa, Fla.
Professional Disposables International, Nice-Pak Products Inc, Orangeburg, NY.
McCormick green food color, McCormick and Co Inc, Hunt Valley, Md.
Olympus n-Stream G3 SD image capture unit, Olympus America Inc, Center Valley, Pa.
Royal Canin Gastrointestinal Low Fat canned diet, Royal Canin USA Inc, St Charles, Mo.
Hill's Science Diet Canine Adult Maintenance, Hill's Pet Nutrition Inc, Topeka, Kan.
Giraldo LF, Leal LR, Leon GA, et al. Systematic review and metaanalysis of the accuracy of flexible endoscopic evaluation of swallowing (FEES) and videofluoroscopic swallowing study (VFSS) for the diagnosis of oropharyngeal dysphagia in adults (abstr). Am J Respir Crit Care Med 2013;187:A5678.
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Appendix 1
Scores for ease of placement of an endoscope in the nasopharynx of dogs to allow visual assessment of swallowing.
| Scores | Description |
|---|---|
| 1 | Easy placement of the tip of the endoscope into the nasopharynx with no or minimal resistance by the dog and only a single attempt required for successful placement. |
| 2 | Relatively easy placement of the tip of the endoscope into the nasopharynx with minimal resistance by the dog (2 or 3 episodes of head shaking during nasal passage of the endoscope) and 2 attempts required for successful placement. |
| 3 | Moderately easy placement of the tip of the endoscope into the nasopharynx with moderate resistance by the dog (4 or 5 episodes of head shaking and 2 or 3 attempts to stand during nasal passage of the endoscope) and 3 attempts required for successful placement. |
| 4 | Challenging placement of the tip of the endoscope into the nasopharynx because of a lack of compliance of the dog (repeated shaking of the head or repeated sneezing to dislodge the endoscope [or both] and repeated attempts to stand during nasal passage of the endoscope), the need for an additional technician to provide restraint of the dog, and 4 attempts required for successful placement. |
| 5 | Difficult placement because of a lack of compliance by the dog, the need for an additional technician to provide restraint, and ≥ 5 attempts for successful endoscopic placement. |
Appendix 2
Scores for tolerance of placement of an endoscope in the nasopharynx of dogs to allow visual assessment of swallowing.
| Scores | Description |
|---|---|
| 1 | Procedure tolerated well and the dog required minimal restraint and offered minimal resistance after placement of the endoscope; dog maintained a sitting posture, and there were no episodes of head shaking during the procedure. |
| 2 | Procedure tolerated well with minimal resistance by the dog characterized as 1 or 2 episodes of head shaking after placement of the endoscope in the nasopharynx. |
| 3 | Procedure tolerated moderately well with some resistance by the dog characterized as 3 or 4 episodes of head shaking after placement of the endoscope in the nasopharynx. |
| 4 | Procedure tolerated minimally with resistance by the dog characterized as ≥ 5 episodes of head shaking, sneezing, and attempting to stand after placement of the endoscope in the nasopharynx; an additional technician was needed to restrain the dog and maintain the endoscope in the nasopharynx. |
| 5 | Procedure poorly tolerated with severe resistance by the dog characterized as repeated head shaking, sneezing, and attempting to stand after placement of the endoscope in the nasopharynx; an additional technician was needed to help restrain the dog and keep it in a sitting position. |
