Abstract
Background
Clinical evaluation of alar fold (AF) collapse is presently based upon subjective evaluation of improvement in breathing and respiratory noise after suturing the AFs dorsally.
Objectives
To evaluate use of nasopharyngeal airway pressure (NAP) as an objective method of assessing for the presence of AF collapse during exercise. NAPs should also potentially provide a precise means to grade the degree of airway obstruction present and response to surgical treatment.
Study Design
Prospective clinical study of actively racing Standardbred horses.
Methods
Standardbreds undergoing this test were outfitted with a heart rate monitor and warmed up on the treadmill for approximately 2000 m, prior to instrumentation with the analogue pressure sensor positioned in the nasopharynx. NAPs were measured continuously before and after the AFs were temporarily sutured dorsally, when horses were trotted at a heart rate ≥200 bpm for 2 min under identical testing circumstances. Peak inspiratory and expiratory NAPs were determined for each horse. A two‐way repeated measures ANOVA was performed to analyse the effect of suturing the AFs dorsally on inspiratory and expiratory NAPs. When possible, horses were tested again after AF resection surgery.
Results
Twenty‐one consecutive cases with suspected AF collapse were tested. Suturing the AFs dorsally had a significant effect on expiratory NAPs (p < 0.001), but not on inspiratory NAPs. Expiratory NAPs decreased from baseline (mean ± SD) 35.8 ± 8.81 cmH2O to 20.1 ± 7.04 cmH2O after suturing AFs dorsally; to 13.3 ± 2.29 cmH2O after complete AF resection in 13 available horses.
Main Limitations
Not all horses were available for NAP testing post‐operatively.
Conclusions
NAP measurements provided a precise objective means to determine whether a horse was affected with AF collapse and assess improvement in airway function after surgery. AF collapse caused a moderate to marked expiratory airway obstruction in many affected racehorses.
Keywords: airway pressure measurement, alar fold, horse, upper respiratory tract obstruction
Zusammenfassung
Hintergrund
Die klinische Beurteilung eines Kollapses der Flügelknorpel (AF) basiert derzeit auf der subjektiven Einschätzung einer Verbesserung der Atmung und der Atemgeräusche nach dorsaler Fixierung der Flügelknorpel durch Nähte.
Ziele
Die Verwendung des nasopharyngealen Atemwegsdrucks (NAP) sollte als objektive Methode zur Beurteilung eines Flügelknorpelkollapses während der Belastung untersucht werden. Zudem könnten NAP‐Messungen eine präzise Einschätzung des Ausmaßes der Atemwegsobstruktion sowie der Reaktion auf eine chirurgische Behandlung ermöglichen.
Studiendesign
Prospektive klinische Studie an aktiv rennenden Standardbred‐Trabern.
Methoden
Die getesteten Traber wurden zunächst mit einem Herzfrequenzmesser ausgestattet und auf dem Laufband über ca. 2000 Meter aufgewärmt. Anschließend wurde ein analoger Drucksensor im Nasopharynx platziert. NAPs wurden kontinuierlich gemessen – vor und nach dorsaler Fixierung der Flügelknorpel – während die Pferde bei einer Herzfrequenz ≥ 200 bpm für 2 Minuten unter identischen Bedingungen trabten. Für jedes Pferd wurden die maximalen inspiratorischen und exspiratorischen NAPs ermittelt. Zur Analyse des Effekts der dorsalen Fixierung auf die inspiratorischen und exspiratorischen NAPs wurde eine zweifaktorielle ANOVA mit Messwiederholung durchgeführt. Wenn möglich, wurden die Pferde nach chirurgischer Entfernung der Flügelknorpel erneut getestet.
Resultate
21 aufeinanderfolgende Fälle mit Verdacht auf Flügelknorpelkollaps wurden getestet. Die dorsale Fixierung der Flügelknorpel hatte einen signifikanten Einfluss auf die exspiratorischen NAPs (p < 0,001), jedoch nicht auf die inspiratorischen NAPs. Die exspiratorischen NAPs sanken vom Ausgangswert (Mittelwert ± SD) 35,8 ± 8,81 cmH2O auf 20,1 ± 7,04 cmH2O nach dorsaler Fixierung und auf 13,3 ± 2,29 cmH2O nach vollständiger chirurgischer Entfernung bei 13 verfügbaren Pferden.
Wichtigste Einschränkungen
Nicht alle Pferde standen für eine postoperative NAP‐Messung zur Verfügung.
Schlussfolgerungen
NAP‐Messungen ermöglichen eine präzise und objektive Bestimmung eines Flügelknorpelkollapses sowie eine Beurteilung der Verbesserung der Atemwegsfunktion nach operativem Eingriff. Ein Flügelknorpelkollaps führte bei vielen betroffenen Rennpferden zu einer moderaten bis ausgeprägten exspiratorischen Atemwegsobstruktion.
1. INTRODUCTION
Exercise‐induced upper respiratory tract (URT) disorders at the level of the nares/nasal passageways in horses are much less commonly reported relative to disorders involving the pharyngeal/laryngeal regions and are potentially under‐diagnosed. 1 More than 50% of the total URT airway resistance has been attributed to the level of the nares and nasal passageways in normal horses. 2 Since the horse is an obligate nasal breather, due to the unique conformation of the soft palate in this species, it cannot switch to mouth breathing during exercise as other mammals, including humans. Horses therefore cannot avoid the high airway pressure gradients associated with nasal breathing, and this predisposes the horse to problems within the URT 3 and potentially in the region of the nares.
The external nares of the horse are large and dilation of the nares is achieved by contraction of four different muscles: lateralis nasi, caninus, dilator naris apicales and levator nasolabialis. 4 The nares are supported by the alar cartilages dorsally, which divide the external nares into the ventral nostril leading to the nasal passageway and the dorsal diverticulum or false nostril. 5 Dynamic collapse of the external lateral nares, or alar folds (AF), was first described by Foerner in 4 American Saddlebred horses. 6 This was typically recognised as flutter/filling of the false nostrils, producing a persistent characteristic noise and vibration from the external nares during exercise. Alar fold collapse has been diagnosed most frequently in American Saddlebreds 6 and Standardbreds 7 , 8 but occurs also sporadically in other breeds of horses such as Thoroughbreds. 1 , 9 The surgical treatment for AF collapse originally described by Foerner 6 is the foundation for today's technique of AF resection, which has been further refined by Hawkins et al. 7 More recently, a technique for AF resection in standing, sedated horses has been described 10 using local anaesthesia and a bipolar dividing and vessel sealing device (LigaSure™).
Clinical evaluation and diagnosis of AF collapse is presently based upon subjective evaluation of improvement in breathing and respiratory noise after suturing the AFs dorsally, thereby preventing air from entering and filling the nasal diverticulum during inspiration. 6 , 11 There is limited information in the literature about the degree of upper airway obstruction created by exercise‐induced abnormalities in the region of the external nares/nostrils of horses, and many individuals present mainly due to the persistent and undesirable noise from this region during moderate to strenuous exercise. The condition needs to be distinguished from ‘high blowing’ which is an intermittent fluttering noise from the region that is periodically present if the horse is frightened or after strenuous exercise.
There is a need for more objective methods of evaluating upper airway mechanics in horses beyond videoendoscopy to clinically determine whether an individual horse has an upper airway obstruction; whether it is inspiratory, expiratory, or both in nature; and the degree of its magnitude. 3 , 12 , 13 Unjustified surgery of the nostril region is one of the stated prohibited procedures by the European Trotting Union (https://www.uet-trot.eu/en/documentation). Since clinical evaluation of AF collapse is presently subjective at best, there is a need to develop an objective screening test for this condition.
There is also a need for more objective methods for assessing response to surgery or other treatments instigated. Evaluating post‐operative racing data has been the most common method of assessing response to intervention in racehorses with upper airway abnormalities but is to date poorly standardised and can be influenced by many other factors, including the development of new performance‐related problems in the same or other body systems. 14 , 15 , 16
We hypothesised that measurement of nasopharyngeal airway pressures (NAP) would provide an objective means to determine the type and degree of upper airway obstruction present in an individual horse and that these pressure values could be used to accurately document the improvement obtained (or not) after surgical treatment. The main goal of this study was therefore to investigate whether measurement of NAP before and after suturing the AFs dorsally would provide an objective and definitive method of assessing horses for the presence of AF collapse during strenuous exercise, and to assess improvement obtained following complete surgical resection of the AFs.
2. MATERIALS AND METHODS
2.1. Study population
Active trotting Standardbred racehorses that had undergone a standardised high‐speed treadmill videoendoscopy (HSTV) on an outpatient basis at our hospital between March 2019 and August 2023, that demonstrated evidence of continuous false nostril filling and abnormal respiratory noise from the region of the external nares during the test, were enrolled in this prospective clinical study. These horses underwent the AF protocol the same day or within a 2‐week period of the HSTV. Additionally, Standardbreds referred to our hospital specifically for objective evaluation of the AF region (only) due to obvious clinical signs of this disorder during training were included. Finally, control Standardbreds were recruited following presentation by trainers requesting a comprehensive evaluation of respiratory function and in which no evidence of respiratory dysfunction or disease was found.
2.2. High‐speed treadmill protocol and nasopharyngeal pressure measurement
All affected horses included in this study underwent this specific treadmill protocol developed for evaluating racehorses with signs of false nostril flutter and/or suspicion of AF collapse. All horses were outfitted with a halter, lead rope, and heart rate monitor and were warmed up on a high‐speed treadmill (Säto) for approximately 2000 m prior to instrumentation with the nasopharyngeal pressure sensor.
An analogue pressure sensor (Millar Mikro‐Cath™, Millar Inc./AD Instruments) was inserted into a polyethylene tubing (Baxter Scientific Products) with a sealed end and eight small, perforating holes in the distal 8 cm. The pressure sensor was secured to the tubing with the sensor tip at the level of the fourth hole from the sealed end. The pressure sensor and tubing were connected via a control unit (PCU‐2000 Pressure Control Unit, Millar Inc.) to a recording unit (PowerLab 8/35, AD Instruments), which was connected to a laptop with LabChart Pro software (AD Instruments) for real‐time recording and later analysing of the pressure tracings. A two‐point calibration of the pressure sensor was performed immediately prior to measurement in all cases, followed by a one‐point calibration immediately after the exercise test to determine whether any drifting of pressure tracings occurred. Under temporary endoscopic guidance, the catheter/sensor unit was passed through the right nasal passageway and positioned at the level of the right guttural pouch opening. The tubing was fixed to the ventrolateral aspect of the right external nares using a single simple interrupted suture, taking care not to interfere with the AF or lateral margin of the external nares.
Following instrumentation, NAPs were measured continuously for a 2‐min period during high‐speed trotting. The 2‐min period of recording (Video S1) was started once the horses had achieved a heart rate of ≥200 bpm. This exercise level was typically reached at a speed of 9 m/s on a 1.5° treadmill incline. Following the initial 2‐min period of NAP measurements before suturing the AFs, the treadmill was stopped, and the AFs were temporarily sutured dorsally with a single interrupted suture of USP 0 polyglactin 910 with a CPX needle. This was placed approximately 2 cm caudal to the alar cartilage on each side and tied snugly on the dorsal aspect of the nasal bone. 6 , 11 Once the AFs were sutured dorsally, the prior exercise test was repeated with identical settings for another 2 min, commencing once the horse achieved a heart rate ≥200 bpm (Video S2). Peak inspiratory and expiratory NAPs were determined for each horse before and after suturing the AFs dorsally by averaging the values for 10 consecutive breaths during the final 15–45 s of both 2‐min phases of the test. The suture was immediately removed once the test was completed.
2.3. Alar fold resection surgery
In general, we presently grade airway obstructions as: ‘mild’ if the change over the normal expected range in measured airway pressure is less than 10 cmH2O; ‘moderate’ if between ±10 and 20 cmH2O; or ‘marked’ if greater than ±20 cmH2O. All horses diagnosed with AF collapse using NAPs in the current study received complete AF resection surgery if tying the alar folds dorsally improved baseline measured NAP values. Surgery was performed either under general anaesthesia via a 10 cm incision through the lateral ala of the nostril on each side 1 , 7 ; or under standing sedation with bilateral infraorbital nerve blocks using a bipolar dividing and vessel‐sealing device (LigaSure™) via the external nares. 10 With both techniques, a 3–5 cm portion of the ventral conchal cartilage was removed with careful attention placed upon not having any remaining redundant AF tissue or pocket formation at the level of the incisive notch of the premaxilla. 1 , 10 Horses received benzyl penicillin (22,000 IU/kg IV q8h) and flunixin meglumine (1.1 mg/kg IV q24h) for 1–2 days in the perioperative period prior to discharge from the hospital. They thereafter received NSAIDs q24h PO for 3–4 days after discharge. Trainers were instructed to rest the horses from training for 3–4 weeks after surgery and to remove crusts within the rostral nasal passageway once to twice weekly wearing latex gloves using sterile gauze and 0.9% NaCl.
When possible and available, horses that received complete bilateral AF resection surgery with either technique were retested at the hospital post‐operatively for NAPs with the same protocol once they had returned to full race training, or at a later convenient point in time in the horse's racing schedule.
2.4. Data analysis
Data were analysed using RStudio version 2024.04.2 + 764 (Posit Software, PBC). Normality was assessed by inspecting descriptive statistics (histogram, mean, median, skewness) and performing the Shapiro–Wilk test. The assumption of homogeneity of variances was evaluated using Levene's test. Two‐way repeated measures ANOVAs were performed to analyse the effect of suturing the AFs dorsally on inspiratory and expiratory NAPs of all affected horses, to analyse the effect of complete AF resection surgery on inspiratory and expiratory NAPs for all affected horses with post‐operative measurements, and to analyse the effect of suturing the AFs dorsally on inspiratory and expiratory NAPs of unaffected horses/controls. For all ANOVAs, Tukey's post hoc test for pairwise comparisons was performed. Two‐sample t‐tests were performed to compare baseline inspiratory and expiratory NAPs between cases and controls. Level of significance was set at p < 0.05.
3. RESULTS
3.1. Study population
During the study period, 124 active Standardbred racehorses presented for HSTV evaluation at our hospital. Of these, 18 consecutive cases in which we suspected AF collapse were tested using the NAP protocol and included in this study (Figure 1). During the previous HSTV examination, six of these 18 horses were additionally diagnosed with intermittent dorsal displacement of the soft palate (iDDSP), 1 with palatal instability and 1 horse with mild collapse of the roof of the nasopharynx. None of these 18 horses demonstrated laryngeal abnormalities or evidence of lower respiratory tract discharge. In addition, 3 horses were referred to the hospital with obvious signs of AF collapse specifically for the NAP protocol (only). These horses did not receive HSTV. The mean (±SD) age of the 21 affected horses was 4 (±1.55) years. These included 13 females, 5 gelded males and 3 males (Table 1).
FIGURE 1.
Flow chart of cases included in this study. STB, Standardbreds; HSTE, high speed treadmill endoscopy; AFC, alar fold collapse; URT, upper respiratory tract; wnl, within normal limits; NAP, nasopharyngeal airway pressures.
TABLE 1.
Signalment and data of Standardbred racehorses affected by alar fold collapse (n = 21); with mean inspiratory and expiratory nasopharyngeal airway pressures (cmH2O) obtained before and after suturing the alar folds dorsally and post‐operatively when available (n = 13).
| No. | Age | Sex | Inspiratory NAP (cmH2O) | Expiratory NAP (cmH2O) | Time from surgery to post‐op evaluation (months) | ||||
|---|---|---|---|---|---|---|---|---|---|
| Before suturing AFs | After suturing AFs | Post‐operative | Before suturing AFs | After suturing AFs | Post‐operative | ||||
| 1 | 4 | F | −15.1 | −17.7 | – | 54.3 | 34.0 | – | – |
| 2 | 6 | F | −19.2 | −17.1 | −23.0 | 40.6 | 20.9 | 12.3 | 5.3 |
| 3 | 8 | MG | −15.9 | −17.7 | – | 31.1 | 16.5 | – | – |
| 4 | 3 | F | −22.9 | −21.9 | – | 31.7 | 29.1 | – | – |
| 5 | 2 | F | −16.9 | −17.4 | −17.2 | 36.8 | 21.4 | 11.1 | 29.2 |
| 6 | 4 | MG | −8.2 | −6.4 | – | 30.8 | 11.1 | – | – |
| 7 | 3 | F | −20.6 | −23.1 | – | 31.5 | 22.4 | – | – |
| 8 | 3 | MG | −9.1 | −12.5 | −9.6 | 48.6 | 19.4 | 17.2 | 19.4 |
| 9 | 6 | M | −9.5 | −11.7 | – | 20.4 | 7.1 | – | – |
| 10 | 4 | F | −14.2 | −9.3 | −12.7 | 40.1 | 17.6 | 12.7 | 3.8 |
| 11 | 4 | F | −12.6 | −17.8 | −16.6 | 20.8 | 15.6 | 11.8 | 9.4 |
| 12 | 4 | F | −14.7 | −16.9 | – | 29.4 | 25.1 | – | – |
| 13 | 6 | M | −22.4 | −16.5 | −17.3 | 44.2 | 25.6 | 11.6 | 5.3 |
| 14 | 3 | F | −14.8 | −16.3 | −10.6 | 36.3 | 19.9 | 17.5 | 6.1 |
| 15 | 5 | F | −9.5 | −11.3 | −7.2 | 45.7 | 18.1 | 14.3 | 2.0 |
| 16 | 3 | M | −24.9 | −17.3 | −19.1 | 39.0 | 28.0 | 12.1 | 8.9 |
| 17 | 4 | F | −16.0 | −21.5 | −15.5 | 46.0 | 31.6 | 14.9 | 9.4 |
| 18 | 3 | MG | −14.5 | −15.8 | −21.2 | 29.4 | 14.0 | 9.8 | 1.4 |
| 19 | 7 | F | −12.2 | −16.2 | −12.3 | 33.5 | 19.6 | 14.5 | 4.3 |
| 20 | 3 | F | −16.0 | −18.6 | – | 26.5 | 15.2 | – | – |
| 21 | 4 | MG | −21.3 | −19.2 | −19.9 | 35.3 | 9.9 | 12.5 | 4.6 |
Note: There was a significant (p < 0.001) reduction in expiratory nasopharyngeal pressures after suturing the alar folds dorsally (compared with before suturing) and a further a significant (p = 0.003) reduction in expiratory nasopharyngeal pressures post‐operatively (compared with after suturing). There were no significant changes in inspiratory nasopharyngeal pressures.
Abbreviations: AF, alar fold; F, female; M, male; MG, male gelded; NAP, nasopharyngeal pressure.
In all affected horses, AF collapse was bilateral and visually appeared to be bilaterally symmetrical. The condition was continuously present in all horses during exercise from moderate to faster speeds (Video S1). Although the severity of clinical signs of AF collapse varied from horse to horse, suturing the AF dorsally subjectively seemed to make breathing easier and decreased the regional abnormal noise production by ca. 70–80% in all horses included in the study (Video S2).
Eight clinically normal Standardbreds with no evidence of URT obstruction during the previous HSTV were tested to establish regional baseline values for NAP in our population of racehorses. The horses' trainers wished for them to also be evaluated for this condition while examined at our hospital. Five of these 8 control horses had NAPs also measured after tying the AFs dorsally. Their signalment and data are presented in Table 2. Their mean (±SD) age was 4 (±1.39) years.
TABLE 2.
Signalment and data of normal Standardbred racehorses with no URT abnormalities (n = 8) with inspiratory and expiratory nasopharyngeal airway pressures (cmH2O) obtained before ± after suturing the alar folds dorsally (n = 5).
| No. | Age | Sex | Inspiratory NAP (cmH2O) | Expiratory NAP (cmH2O) | ||
|---|---|---|---|---|---|---|
| Before suturing AFs | After suturing AFs | Before suturing AFs | After suturing AFs | |||
| 1‐N | 4 | MG | −13.3 | −12.7 | 5.5 | 12.9 |
| 2‐N | 7 | MG | −18.7 | −20.1 | 5.7 | 11.7 |
| 3‐N | 5 | F | −12.4 | −14.5 | 7.9 | 8.4 |
| 4‐N | 4 | F | −23.8 | – | 9.5 | – |
| 5‐N | 3 | F | −6.5 | −7.0 | 10.1 | 10.5 |
| 6‐N | 3 | M | −7.6 | – | 7.9 | – |
| 7‐N | 3 | M | −17.6 | −18.3 | 10.2 | 9.7 |
| 8‐N | 5 | MG | −15.2 | – | 11.6 | – |
Abbreviations: AF, alar fold; F, female; M, male; MG, male gelded; URT, upper respiratory tract; NAP, nasopharyngeal pressure.
3.2. Nasopharyngeal pressure measurements
Suturing the AFs dorsally led to a significant reduction in expiratory NAPs (p < 0.001) of all individually affected horses from a group mean value of 35.8 cmH2O before suturing to a group mean value of 20.1 cmH2O after suturing (Tables 1 and 3). There was no significant change in inspiratory NAPs of affected horses. For five of the eight unaffected control horses enrolled in the study, expiratory NAP changed from a group mean value of 8.6 cmH2O before suturing to a group mean value of 10.6 cmH2O after suturing the AFs dorsally (Tables 2 and 3). Neither the change in inspiratory nor expiratory NAPs of control horses after suturing the AFs dorsally was statistically significant. When comparing the baseline (before suturing) NAPs of affected horses and controls, there was a significant difference in baseline expiratory NAPs (p < 0.001), but not in baseline inspiratory NAPs (Table 3).
TABLE 3.
Summary of mean (±SD) inspiratory and expiratory nasopharyngeal airway pressures (cmH2O) before and after suturing the alar folds dorsally in unaffected and affected horses, and post‐operatively in available affected horses.
| Number of horses | Inspiratory NAP (cmH2O) | Expiratory NAP (cmH2O) | ||
|---|---|---|---|---|
| Unaffected horses | Before suturing AFs | n = 8 | −14.4 (±5.8) | 8.6 (±2.2)* |
| After suturing AFs | n = 5 | −14.5 (±5.1) | 10.6 (±1.8) | |
| Affected horses | Before suturing AFs | n = 21 | −15.7 (±4.8) | 35.8 (±8.8)* |
| After suturing AFs | n = 21 | −16.3 (±4.1) | 20.1 (±7.0) | |
| Post‐operatively | n = 13 | −15.5 (±4.8) | 13.3 (±2.3) |
Note: In affected horses there was a significant (p < 0.001) reduction in expiratory nasopharyngeal pressures (marked as bold) after suturing the alar folds dorsally (compared with before suturing) and a further significant (p = 0.003) reduction in expiratory nasopharyngeal pressures post‐operatively (compared with after suturing). There was a significant (p < 0.001) difference in baseline expiratory nasopharyngeal pressures before suturing the alar folds dorsally between unaffected and affected horses (marked with asterisk).
Abbreviations: AF, alar fold; NAP, nasopharyngeal pressure.
3.3. Post‐operative evaluation of Standardbreds affected by alar fold collapse
All 21 horses affected by AF obstruction underwent complete bilateral AF resection surgery. Horses enrolled in the study from 2019 to 2020 were operated on using the open technique under general anaesthesia (n = 2), whereas horses enrolled after 2020 were operated standing using the bipolar dividing and vessel sealing device (n = 19). None of these 21 horses experienced post‐operative complications of note after discharge from the hospital the same or following day. These horses did not receive any additional URT surgical procedures before or after discharge from the hospital. Thirteen of the 21 affected Standardbreds were available for re‐testing post‐operatively, ranging from 1.4 to 29.2 months after surgery (Table 1). All individuals demonstrated further statistically significant reduction/improvement (p = 0.003) in their mean expiratory NAPs from a group mean of 20.1 cmH2O measured initially when the AFs were sutured dorsally to a group mean of 13.3 cmH2O measured post‐operatively (Tables 1 and 3).
4. DISCUSSION
Alar fold collapse in horses, which up to now has been a very subjective diagnosis in veterinary medicine, can be definitively diagnosed with NAP measurements. This study confirms that AF collapse caused an expiratory airway obstruction in the nasopharynx in each of the 21 individually tested racehorses (Table 1). There was no measured effect on inspiratory NAPs (Tables 1 and 3). Many horses tested had moderate to marked airway obstruction upon presentation, raising welfare concerns since this condition is probably underdiagnosed worldwide or considered mainly a cosmetic issue. Suturing the AFs dorsally, thereby closing the entrance of the false nostril, significantly improved expiratory NAPs. Complete bilateral AF resection surgery further improved expiratory NAPs to near normal baseline levels in all 13 horses available for retesting after surgical treatment and return to race training. This confirms the expiratory obstruction originally measured originates from this region.
Baseline expiratory NAPs in 8 active Standardbred racehorses without clinical evidence of AF obstruction or any other URT abnormality ranged from 5.50 to 11.60 cmH2O (Table 2). All horses were tested at the trotting gait with the same protocol used for testing the AF affected individuals. We presently consider 15 cmH2O as the upper limit for mean baseline expiratory NAP in normal Standardbreds based upon review of all our data acquired from this study. Higher baseline expiratory NAPs than this can indicate airway obstruction in the region. We presently have no other diagnosis in this region that causes elevation of the expiratory pressures apart from AF collapse. We presently recommend corrective surgery for those individuals with elevated expiratory baseline NAPs and improvement in expiratory NAPs of at least 5–10 cmH2O after suturing the AFs dorsally.
The results of suturing the AFs dorsally subjectively improved respiration and reduced local respiratory noise by 70–80% in all affected horses. This could be easily assessed standing within 1–2 m of the horse's head while it was undergoing the exercise testing protocol (Videos S1 and S2). The improvement in expiratory NAPs after suturing varied between horses (Table 1) which is probably a reflection of each horse's local anatomy and degree of airway obstruction present, and also our effectiveness in placing secure tight sutures to fully lift the AFs out of the airway. With increased experience, we became more effective at this task during the course of this study.
Based upon this study and data acquired from other ongoing studies, we categorise different forms of URT obstruction: as inspiratory/expiratory or combined; and as mild, moderate or marked. Eleven of the 21 horses diagnosed with AF collapse with this protocol had baseline expiratory pressures prior to suturing the AFs dorsally between 35.0 and 54.3 cmH2O, indicating marked expiratory airway obstruction (Table 1).
Airway pressure measurements in horses were first performed in North America in the 1990s 12 , 17 , 18 and have been to date mainly employed in scientific studies investigating the airway dynamics 13 , 19 , 20 or scientific modelling 21 , 22 of specific URT disorders. They have also been used to objectively measure the effect of tack/equipment interventions 4 , 23 , 24 on horses. The repeatability of pharyngeal and tracheal pressure measurement in horses has also been previously reported. 12 The current study sought to develop airway pressure measurement as an objective outpatient clinical tool in client‐owned patients. The sensor in the polyethylene catheter provided a quick and noninvasive method for acquiring objective data regarding local airway function. This provided a better understanding of the disorder, the potential impact on that individual's performance and degree of improvement after AF resection surgery. Previously published studies had already documented improvement in racing performance parameters after AF resection surgery in affected horses. 1 , 7 , 9 , 10
Thirteen of the 21 horses in this study were available for postoperative NAP testing after complete bilateral AF resection. Complete bilateral AF resection surgery further improved mean expiratory NAPs (13.3 ± 2.29 cmH2O) relative to values measured when their AFs were sutured dorsally (Tables 1 and 3). This indicates that either conventional or standing bipolar dividing and vessel‐sealing device surgery is highly effective at restoring air passage through this region in horses suffering from this condition. This was regardless of the highly variable time period of 1.4–29.2 months between surgery and postoperative NAP testing. This indicates that AF resection surgery, when properly performed, provides a permanent long‐term solution to this form of airway obstruction. Surgery with either technique was very reliable.
Suturing the AFs dorsally, thereby closing the entrance of the false nostril and preventing the filling of air during inspiration, also relieved much of the local expiratory obstruction present, but to a lesser and more variable degree than AF resection surgery (Table 1). This study using NAP measurements also served to validate the historic practice of suturing the AFs dorsally, 6 , 11 to close the entrance to the false nostrils, as a subjective diagnostic test for screening horses for this condition. Suturing the AFs dorsally induced very mild obstruction in all 5 of the normal horses (Table 2) receiving this procedure, indicating that normally functioning horses can more effectively lift the false nostril out of the airway during exercise than our applied sutures. This finding demonstrates that suturing the AFs dorsally, or resecting the AFs, has no benefit in horses not affected with AF collapse. These horses already have very low baseline expiratory NAPs. We did not suture the AF dorsally in the 3 final normal horses since the first 5 horses demonstrated the creation of a mild obstruction with the procedure (Table 2). The important data was obtaining the baseline expiratory NAPs in these 8 horses, which were so low that there could not be a local airway obstruction, making the application of the AF sutures unnecessary.
In the current study, AF collapse caused a moderate to marked expiratory obstruction in many horses as documented by the baseline NAP measurements, which raises welfare concerns as this condition is potentially underdiagnosed. Within the equine URT tract, 50% of the total upper airway resistance resides at the level of the nares and nasal passageways in normal exercising individuals. 2 Additionally, one of the sites of highest airflow velocity and turbulence is found at the caudal nasal passageway since this region has the smallest cross‐sectional area. 25 According to Bernoulli's principle, the Venturi effect and physical laws, obstruction at the level of the nares will theoretically serve as a bottle neck to airflow in the region and thereby predispose to secondary collapse within the nasopharynx. In a previous study including 21 Standardbred racehorses diagnosed with AF collapse, 10 of the individuals were further diagnosed with iDDSP and 2 other individuals had collapse of the roof of the nasopharynx during HSTV. 1 In this study, of the 18 horses which also underwent HSTV at our hospital, six were additionally diagnosed with iDDSP, 1 with palatal instability and 1 horse with mild collapse of the roof of the nasopharynx. The significantly increased regional expiratory NAPs measured in all 21 AF collapse cases in this study may predispose some of these individuals to different forms of nasopharyngeal collapse by a presently unknown mechanism. On that note, it is interesting that iDDSP is also mainly an expiratory obstruction 13 , 26 as most other obstructions in the equine URT, especially at the level of the larynx, are mainly inspiratory in nature. In our hospital, we treat the AF collapse with complete bilateral resection surgery, and it is our subjective opinion that the other nasopharyngeal conditions often seem to improve once proper airflow through the nasal passageway is restored.
Our NAP measuring protocol considers that complex URT collapse is common in harness racehorses. If one places the pressure measuring system in the trachea, then one evaluates the entire URT from nostrils to rostral trachea for cumulative inspiratory and/or expiratory obstructions. By having the unit positioned in the nasopharynx, one is just evaluating the region from the nostrils to rostral nasopharynx. Since AF collapse is continuously present even at submaximal exercise efforts, we exercise the horses on a slight incline for 2‐min periods at a heart rate of 200 bpm, which seems to be approximately a 90% effort for most individuals. By having short submaximal periods of exercise/pressure recording, we avoid inducing secondary nasopharyngeal collapse. If secondary collapse did occur, it would be noticed on our continuous 2‐min chart tracing of pressures (Figure 2) either before or after tying the AFs dorsally. For example, iDDSP would cause a lowering of expiratory NAP readings since airflow is reduced and partially diverted to the oral cavity. 13 None of the 21 horses tested with the AF diagnostic protocol, or the 13 horses tested after AF surgery, had evidence of other secondary airway collapse on their respective 2‐min chart tracings which had consistent inspiratory and expiratory pressure peaks (Figure 2).
FIGURE 2.
Compressed 2‐min tracings: of baseline inspiratory and expiratory pressures measured before (left); and after tying the alar folds dorsally (right) in a horse diagnosed with alar fold collapse. Each positive pressure spike is peak expiration for a single breath and the negative spikes are peak inspiration for a breath. The nasopharyngeal airway pressures are measured in cmH2O.
Performing NAP measurements in horses suspected to have abnormal function of the nostrils or nasal passageways shows great promise as an objective clinical tool to identify horses with suspected obstruction in this region. It also provides a direct, precise clinical means to assess the degree of response to surgical or other treatment forms. Up to now, racing performance parameters have historically been used for this purpose in equine veterinary medicine. Racing performance data has been used in 100 s of scientific publications as an indicator of return to original baseline fitness level after diagnosis/treatment of upper respiratory tract, orthopaedic or other problems, but can introduce many confounding factors. 14 , 15 , 16 Historically, there is no consensus for which parameters are best used. This can also vary with the different forms and traditions of horse racing in different geographical regions. More importantly, horses can often have concurrent undiagnosed performance problems or acquire new problems during training in the post‐treatment period, which can affect the perception of success of a veterinary intervention. 27 Horses can also return to racing, but at a lower level of racing class, which also further confounds results. Upper airway pressure measurements, such as NAPs, provide quantifiable numerical data in the isolated region of interest, readily amenable to statistical analysis as performed in this study.
Limitations of this study include the small sample size of AF collapse affected racehorses and controls and that not all operated horses were available for post‐operative NAP testing. This form of testing also presently requires a high‐speed treadmill and pressure measuring equipment, making it most suitable for large practices or university hospitals. The AF suturing technique can vary between horses in effectiveness in lifting and closing the entrance to the false nostril and thereby minimising the expiratory obstruction (Table 1). However, the results of complete AF resection surgery were very consistent in this study group, with post‐operative expiratory NAPs ranging from 9.8 to 17.5 cmH2O in the 13 horses tested after surgery (Table 1).
Human medicine has recently taken interest in airway pressure measuring technology, first used in equine veterinary medicine, 12 , 17 , 18 in the treadmill videoendoscopic evaluation of exercised induced laryngeal obstruction (EILO) in their patients. Human medicine also has a great need to validate their diagnoses and treatments and assess precisely the degree of airway impairment present before and after treatment. The first airway pressure studies in human medicine have now been recently published utilising this technology first developed in horses. 28 , 29 Though videoendoscopic evaluation during exercise allows for diagnosis and subjective grading of the degree of URT collapse in horses and humans, airway pressure measurements provide supplementary objective numerical data which allows for definitive evaluation of type and magnitude of airway obstruction. Airway pressure measurements hold the promise of 1 day becoming as important to respiratory tract medicine as blood pressure measurements have become in cardiology. This study verifies the usefulness of this airway measuring technology in the diagnosis of this form of URT disorder, in grading the degree of severity of obstruction in individuals and in objectively determining the improvement obtained with surgery in active Standardbred racehorses.
FUNDING INFORMATION
This study was supported by the Norwegian Research Council (NFR) grant # 311955 and the Swedish‐Norwegian Foundation for Equine Research grant # H‐19‐47‐472.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
AUTHOR CONTRIBUTIONS
Eric Strand: Conceptualization; investigation; funding acquisition; writing – original draft; visualization; project administration; supervision; data curation; writing – review and editing. Hanna Vermedal: Writing – original draft; visualization; formal analysis; investigation; data curation; writing – review and editing. Hanna Margrethe Berg Olsen: Investigation; writing – review and editing; data curation. Cathrine Taule Fjordbakk: Conceptualization; investigation; writing – review and editing; data curation. Zoe Louise Fretheim‐Kelly: Writing – review and editing; investigation; conceptualization; funding acquisition; data curation.
DATA INTEGRITY STATEMENT
Eric Strand and Hanna Vermedal had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of data analysis.
ETHICAL ANIMAL RESEARCH
Research ethics committee oversight not currently required by this journal: procedures were performed as part of clinical investigations.
INFORMED CONSENT
Explicit owner consent for inclusion of animals in this study was not obtained. Owners/trainers were made aware that case information may be used for research in general.
Supporting information
Video S1. Baseline evaluation of a Standardbred racehorse moderately affected with alar fold collapse. Note the abnormal fluttering noise.
Video S2. The same horse 5 min later after tying up the alar folds. Note the subjective improvement in air passage and reduction in abnormal respiratory noise from the region.
ACKNOWLEDGEMENTS
We thank the equine treadmill team at the Norwegian University of Life Sciences for help driving the horses during the treadmill protocol: Marius Holm, Jessica Gunnulfsen and Diana Olsson.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are openly available at https://data.mendeley.com/datasets/4h7jnhwvyz/1.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Video S1. Baseline evaluation of a Standardbred racehorse moderately affected with alar fold collapse. Note the abnormal fluttering noise.
Video S2. The same horse 5 min later after tying up the alar folds. Note the subjective improvement in air passage and reduction in abnormal respiratory noise from the region.
Data Availability Statement
The data that support the findings of this study are openly available at https://data.mendeley.com/datasets/4h7jnhwvyz/1.