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Upper Airway: Clinical Perspectives
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The stability of the equine upper airway is critical to the performance of horses competing at maximal exercise intensity and to the production of normal respiratory sounds at both sub-maximal and maximal exercise intensity. In a review of the last 5 years (2000-2004) 237 horses were presented for poor performance evaluation at the Equine Hospital of the Cornell University Hospital for Animals. The diagnosed cause for the presentation of the horses was respiratory obstruction in 76% of the horses (50% of them dorsal displacement of the soft palate [DDSP]). In our practice, it appears that either the prevalence or recognition of upper airway disease in horses is increasing. Alternative interpretations might include that there has been a decrease in the incidence of orthopedic injuries due to enhanced training techniques or track surfaces and earlier recognition or better prevention of factors contributing to the occurrence of abdominal disorders.
The equine clinician faces multiple challenges in reconciling/integrating the advances in our understanding of the etiopathogenesis, diagnosis, and treatment of horses affected by various upper airway abnormalities. Indeed, most advances have been with an abnormality experimentally created in horses that originally had normal airways. Furthermore, many conclusions are based on horses exercising at maximal heart rate rather than at the speed they compete. For example, an area of critical interest to clinical practices is diagnosing horses with a complaint of upper airway noise during exercise. The clinician must make a prediction based on a physical exam at rest and perhaps observation during exercise. The challenge is greater if the horse has a normal upper airway at rest and an upper airway abnormality at exercise (i.e., dynamic airway obstructions). Furthermore, the clinician must predict the general presence and severity of upper airway obstruction based on a resting exam. Sometimes, the clinician is asked to make a prediction based on a resting exam made 1 to 2 years before the horse started its competitive career (i.e., from yearling sales). After a thorough physical exam of the upper airway, videoendoscopy has been the gold standard for diagnosing an upper airway abnormality. The recognition of recurrent laryngeal neuropathy (RLN) can be made at rest by a relatively accurate means. The revised consensus laryngeal grade (Havermeyer Symposium, September 2003) is shown in Figure 1:
Figure 1. Havemeyer Consensus grading system of laryngeal function performed in the standing unsedated horse † | ||
Grade | Description | Sub-Grade Description |
I | All arytenoid cartilage movements are synchronous and symmetrical and full arytenoid cartilage abduction can be achieved and maintained. | - |
II | Arytenoid cartilage movements are asynchronous and/ or asymmetrical but full arytenoid cartilage abduction can be achieved and maintained. | 1. Transient asynchrony, flutter or delayed movement is seen. 2. There is asymmetry of the rima glottidis much of the time due to reduced mobility of the affected arytenoid and vocal fold, but there are occasions, typically after swallowing or nasal occlusion, when full symmetrical abduction is achieved and maintained. |
III | Arytenoid cartilage movements are asynchronous and/ or asymmetrical but full arytenoid cartilage abduction cannot be achieved and maintained. | 1. There is asymmetry of the rima glottidis much of the time due to reduced mobility of the arytenoid and vocal fold, but there are occasions, typically after swallowing or nasal occlusion, when full symmetrical abduction is achieved but not maintained. 2. Obvious arytenoid abductor deficit and arytenoid asymmetry. Full abduction is never achieved. 3. Marked but not total arytenoid abductor deficit and asymmetry with little arytenoid movement. Full abduction is never achieved. |
IV | Complete immobility of the arytenoid cartilage and vocal fold. | - |
† Description generally refers to the left arytenoid cartilage in reference to the right. However, this grading system can apply to the right side (i.e., right grade III-1) |
Although the accuracy of the subgrades has not been validated to date, the following observations were made in a review of 461 horses with a correlation of resting and exercising grade. All 201 horses with laryngeal grade I had normal arytenoid abduction at exercise. 96% of the 114 horses with laryngeal grade II had normal arytenoid abduction at exercise. 80% of the 126 horses with laryngeal grade III had some degree of arytenoid and/or vocal cord collapse at exercise. 100% of the 17 horses with laryngeal grade IV had laryngeal collapse at exercise. This correlates with a recent evaluation of yearlings (Stick et al.) [1], in which horses with a laryngeal grade of I and II had significantly better earnings than horses with a laryngeal grade of III.
Critical new information has been acquired in recent elegant studies that allow one to use sound recording at exercise to confirm a diagnosis [2-4]. This new information gives us a diagnostic alternative in the investigation of a complaint of an abnormal upper airway sound and new practical information in selection of surgical treatment. For example, Brown et al., have indicated that horses with RLN have abnormal frequency bands during inhalation and have a characteristic "sound signature". It is less clear whether the identification of these formats allows arytenoid cartilage collapse and vocal cord collapse to be differentiated from axial deviation of the aryepiglottic folds (see Dr. Derksen’s presentation). Works from both Franklin et al. and Derksen et al. show that horses with DDSP have abnormal frequencies detected during exhalation. This is particularly useful since Parente et al. [5] has documented that there is not a good correlation between resting exam and the presence of DDSP at exercise. These latter two factors complicate the clinician’s diagnosis of palate displacement, leading to over or under recognition of this disease if a treadmill exam is not performed. Sound analysis gives us a way to diagnose this condition, which may occur only during strenuous exercise. A drawback is that some horses with DDSP do not have this abnormal spectrogram. The incidence of these "silent displacers" is unknown, but the author’s clinical impression is that it is around 20%. It is unknown if the sound signature of horses with DDSP can be differentiated from that of horses with epiglottic entrapment. This is largely irrelevant if both diagnostic modalities are used (sound analysis during exercise and endoscopic exam at rest or after exercise).
On the therapeutic side, sound analysis has validated the use of ventriculectomy as a "sound reducing treatment" for horses with RLN and has reinforced the enhanced value of surgically removing the vocal fold to normalize upper airway sound function. Furthermore, Brown et al. have shown that there is not a good correlation between abnormal upper airway sounds and positions or degree of abduction of the left arytenoid cartilage [3]. Clinically, one should conclude that the persistence of an abnormal upper airway sound after surgical treatment does not indicate that there is persistence of airway obstruction. This apparent paradox is consistent with the proven superiority of ventriculocordectomy in restoring normal upper airway sounds compared to laryngoplasty, while the latter normalizes airway mechanics which ventriculocordectomy does not. Those conclusions are true in horses exercising at maximal heart rate, and the author suspects that the same conclusions might not be true in horses performing at 16 to 18 m/s. The persistence of an upper airway sound after surgery is likely an indication of a persistent airway obstruction whose clinical significance is unknown.
Additional Considerations
Recurrent Laryngeal Neuropathy (RLN)
We can recognize this disease with increased accuracy, but the etiology is still unknown. Evidence is mounting that RLN is a heritable disease in the majority of cases. Therefore, it would be preferable to recognize and eliminate the gene(s) responsible for this condition. However, it appears that the disease has a low heritability value or has a wide prevalence given that eliminating the affected patient from the breeding pool has minimal effect on the incidence of this disease (see Dr. Marianne M. Sloet van Oldruitenborgh-Oosterbaan’s presentation).
We can update owners on the prognosis for horses where successful outcome is dependent on improved airway mechanics (see Michael A. Weishaupt’s presentation) or normalization of airway sounds (see Frederik J. Derksen’s presentation). In horses performing at sub-maximal exercise, laryngoplasty restores performance in the great majority of cases [6]. In horses performing at maximal exercise intensity, laryngoplasty is successful, at best, in approximately two thirds of the cases [7]. Partial arytenoidectomy offers a similar clinical outcome in clinical patients yet is an inferior technique in experimental studies [8,9]. However, because both treatments interfere with the protective mechanisms of the larynx, laryngeal reinnervation offers a more physiological approach to treatment with comparable results (see Ian Fulton’s presentation) but with a prolonged delay. The treatment options of RLN need significant improvement. At the more modest level, we need to solve the discrepancy between the position of arytenoid cartilage at surgery and its position 6 weeks later. Do we know the effect of different degrees of abduction on airway mechanics? We know there is not a good correlation between degree of abduction and airway sounds (see Derksen). It appears that we can normalize sounds by bilateral ventriculocordectomy with similar results achieved by unilateral ventriculocordectomy (see Derksen). What about the concomitant presence of contralateral or ipsilateral arytenoepiglottic membrane axial collapse? Should that be treated also? Is it resolved by improving the cross-sectional surface of the rima glottitis?
Chondritis of the Arytenoid Cartilage
Arytenoid chondritis is a disease that affects horses that race or compete on dirt. It is assumed to be secondary to mucosal trauma or inflammation with secondary bacterial invasion of the cartilage stroma. The clinician recognizes early lesions such as ulcers followed by granulomas with and without decreased mobility of the arytenoid cartilage. How does one treat this condition? When is "lumpectomy" chosen over "partial arytenoidectomy" (see Dr. Anderson’s presentation)?
Nasopharyngeal Stability
Recent investigations have greatly increased our understanding of the factors involved in the stability of the nasopharynx. For example, we now know the function of the tensor veli palatinus, the palatopharyngeus and palatinus muscles, as well as that of the stylopharyngeus muscles and their neuromuscular controls (see Dr. Susan Holcombe) [10-14]. Dysfunction of the thyrohyoideus muscle is another cause of nasopharyngeal instability (i.e., DDSP) [15]. Yet direct muscular deficit or indirect muscular dysfunction through the afferent sensory arm can weaken pharyngeal stability. How do we transfer our recent knowledge on the etiopathogenesis of DDSP to a practical setting? How do we recognize that the compliance of the nasopharynx is increased? In clinical cases, specific muscle dysfunction is difficult to diagnose or at least recognize. Specifically, enlargement or inflammation of the structures (i.e., lymph node) in the medial compartment of the guttural pouch is uncommon. On the other hand, pharyngitis is so common in 2-year-olds and early in 3-year-olds’ careers, the incidence of nasopharyngeal instability should be more common. Other factors are important for the stability of the soft palate. Investigations are underway to assess the intrinsic compliance of the soft palate (see Dr. Samantha Franklin’s presentation).
Examination during strenuous exercise does not always allow recognition of DDSP. Why? Proposed explanations include the intermittent nature of this disease, the inability of treadmill exam to mimic the racing condition 100%, and morning training exercise also does not simulate the racing condition 100%. How do we resolve the research findings about the lack of function of the epiglottic cartilage on the occurrence of DDSP, while in clinical cases, epiglottic cartilage abnormality is so commonly associated with DDSP? For example, the absence of DDSP in horses with epiglottic retroversion [14] argues against this structure having a significant role in this condition. How can the absence of DDSP in cases of epiglottic retroversion be reconciled with the association of DDSP with a short epiglottis or subepiglottic masses/cysts? It appears that when epiglottic cartilage is structurally normal in length and appearance, its absence (as in retroversion) does not result in DDSP. Yet, if the epiglottic cartilage is structurally abnormal (subepiglottic mass, epiglottic abscess and epiglottitis), its presence seems to result in DDSP.
In summary, significant critical knowledge has been added in the last 25 years to our understanding of upper airway form and function at exercise. The future should focus on refining our diagnostic tools. We need innovative changes in the treatment of laryngeal hemiplegia. These changes should target maintaining the degree of abduction and be dynamic so that tracheal aspiration of feed material is eliminated. The progress in the equine genome might lead to gene therapy that reverses or prevents the distal axonopathy from affecting the recurrent laryngeal nerve. We need to further increase our understanding of the pathophysiology of certain conditions such as epiglottic entrapment. Can we find a better treatment for arytenoid chondritis through cartilage replacement?
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1. Stick JA, Peloso JG, Morehead JP, Lloyd J, Eberhart S, Padungtod P, Derksen FJ. Endoscopic assessment of airway function as a predictor of racing performance in Thoroughbred yearlings: 427 cases (1997-2000). J Am Vet Med Assoc 2001; 219:962-967.
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