Adherence to treatment recommendations and short-term outcome of pleasure and sport horses with equine asthma

Abstract

Treatments for mild forms of equine asthma are extrapolated from those recommended for severe equine asthma (heaves), but little is known about owner’s adherence to recommendations and treatment efficacy. The objective was to determine which recommendations are implemented by owners and their perception of the clinical response to treatment. Medical records of 43 horses diagnosed with moderate asthma between 2010 and 2012 were retrieved from the Université de Montréal database. Treatments and perceived responses were recorded by telephone survey, 2 to 35 months after diagnosis. All 33 owners who completed the survey attempted to decrease exposure to dust and half had also administered medication. Twenty-four owners (73%) described a > 50% improvement in the clinical signs. There was no association between a specific treatment and outcome. A majority of owners of pleasure and sport horses with equine asthma perceived improvement when limiting exposure to hay and barn dust (alone or with medications).

Introduction

Mild to moderate equine asthma [formerly inflammatory airway disease (IAD); defined as moderate asthma herein] is characterized by cough, excess mucus, and poor performance secondary to inflammation of the lower airways (1). Etiology is incompletely understood but airborne antigens, organic or non-organic dust, previous infections, and pollution might contribute to development of the disease (1). Diagnosis is generally based on the presence of 1 or more compatible clinical signs and evidence of inflammation in bronchoalveolar lavage fluid (BALF). Because clinical signs can be subtle and cough often noticed only during exercise, moderate equine asthma is more likely to be diagnosed in athletic horses. While cytological evidence of airway inflammation can be frequent (sometimes > 70% of horses depending on housing conditions) (2,3), the prevalence of moderate equine asthma (i.e., BALF inflammation with clinical signs) is unknown, especially in pleasure and sport horses. It is likely below the percentage of horses with asymptomatic inflammation and above the estimated prevalence of severe equine asthma or heaves [~15% in temperate climates (4)]. Currently, there are no diagnostic criteria predicting if horses with moderate equine asthma will progress to become severely and chronically affected, and similar treatment approaches are generally recommended.

Current treatment recommendations are extrapolated from those used to control clinical signs in severe equine asthma. They are directed at decreasing exposure to environmental dust particles in conjunction with anti-inflammatory drugs and bronchodilators. Despite strong evidence of efficacy for corticosteroids and antigen avoidance in horses with severe equine asthma (5,6), there is limited information concerning their ability to control milder forms. Only recently dexamethasone and fluticasone were shown to inhibit airway hyper-responsiveness in horses with IAD (7). Clenbuterol was shown to have a transient positive effect on mucociliary clearance and sensitivity to histamine, and sodium cromoglycate improves respiratory scores and stabilizes histamine content of mast cells in horses with moderate equine asthma (IAD) (8–10).

The goals of this study were to evaluate which recommendations (decreased exposure to hay, barn dust reduction, administration of medication) are implemented by owners, to evaluate the perceived clinical response to treatment, and to identify potential factors (age, type of inflammation) influencing short-term outcome (i.e., < 3 y). Specifically, we hypothesized that i) adherence is greater for medication administration than for husbandry recommendations; ii) most pleasure and sport horses diagnosed with moderate equine asthma are perceived to improve with treatment and management; and iii) older horses or horses with BALF neutrophilia are less likely to improve over time.

Materials and methods

Medical records of pleasure and sport horses presented at the Centre Hospitalier Universitaire Vétérinaire of the Université de Montréal between October 2010 and October 2012 for respiratory problems were reviewed. Horses with a final diagnosis of moderate equine asthma based on the presence of compatible clinical signs and BALF inflammation were selected. Inclusion criteria were the presence of 1 or more of the following clinical signs: cough, nasal discharge, or poor performance of at least 3 weeks’ duration in horses engaged in some type of athletic activity other than racing (i.e., no broodmares or retired horses were included). In addition to clinical signs, and based on publications with horses in the same geographic area, lower airway inflammation was identified based on a differential cell count of > 5% neutrophils, ≥ 2% mast cells, or ≥ 1% eosinophils in their BALF (11). Clinical work-up included physical examination, thoracic auscultation with a rebreathing bag, complete blood (cell) count (CBC), upper airway endoscopy, and BALF cytology. When indicated, other causes of poor performance, cough or nasal discharge were ruled out by other ancillary tests (e.g., lameness examination, echocardiography) as deemed appropriate by the attending clinician. Horses with severe equine asthma as well as those with evidence of infectious disease or systemic clinical signs (fever, decreased appetite) were excluded.

Recommendations to clients included i) limiting exposure to hay-associated inhaled antigens by using pelleted, cubed, or pasteurized hay, grass pasture, or silage; ii) husbandry measures to decrease exposure to dust (improving ventilation, increasing turnouts, using low-dust bedding); and iii) administration of inhaled or systemic corticosteroids and bronchodilators. Soaking hay was not part of standard recommendations because most clients had implemented that before presentation and because of the impracticality to combine soaked hay and long turnouts during winter months. At the time of the study, pasteurized hay was not widely available. The use of medication was discussed as an aid to accelerate resolution of clinical signs, improve response if husbandry changes were not sufficient, or if changes in diet and environment could not be implemented. Typical recommendations included short-term oral dexamethasone [starting at 0.05 mg/kg body weight (BW) q24h and decreasing over 2 to 3 wk], inhaled corticosteroids (e.g., fluticasone proprionate, 2 to 3 mg q12 to 24h, tapered off to effect). Bronchodilators were also recommended, including clenbuterol for short oral treatment or inhaled bronchodilators before exercise or in combination with fluticasone.

Owners were invited to answer a standardized questionnaire in the Fall of 2012, 2 to 35 mo (median: 8 mo) after diagnosis. Approximately 1 mo before the telephone interview, clients were contacted by mail to let them know that they would be contacted (unless they declined to be interviewed) and to give them time to gather information on husbandry, medication, and clinical signs. In some cases, we were referred to the person in the best position to answer the questionnaire (caregiver, barn manager, trainer, family member). Initial questions were directed at verifying that the information on signalment, use, and clinical signs were concordant with the medical file. The next set of questions referred to changes in management and treatments that had been implemented since the visit, and if they were permanent or temporary. Finally, clients were asked if they had noticed an improvement or deterioration in the clinical signs (overall and each sign individually). For each sign that had not deteriorated, they were asked to grade improvement from 0% to 100%, 0% being equivalent to “no improvement” and 100% to “complete resolution of clinical signs.” Horses with a reported 50% overall improvement or less were classified as having an unsatisfactory outcome. At the end of the questionnaire, owners were asked their overall satisfaction (“satisfied” or “unsatisfied”) with the outcome. Differences among outcomes for continuous variables were analyzed with Mann-Whitney tests and categorical data were analyzed with Fisher’s exact test. P < 0.05 was considered significant.

Results

Horse population

A total of 43 cases met the inclusion criteria and the questionnaire was completed for 33 cases by 33 owners, for a participation rate of 77%. Horses (19 geldings, 13 mares, 1 stallion) were between 2 and 18 y (median: 6 y) of age and 27 horses were ≤ 10 y old. Quarter Horses and Paint Horses represented 64% of the cases, while Warmbloods and other breeds each represented 18% of the studied population. Quarter Horses and Paint horses were overrepresented compared to their proportion in the hospital population during the same period (35%, P = 0.002). Athletic activities were diverse (e.g., reining, barrel racing, trail riding, dressage) and their use was described as “competitive” (training with the goal of competing) or for “pleasure” by the owners, in 55% and 45% of the cases, respectively. Most horses presented with cough alone or in conjunction with a nasal discharge or poor performance, while only 1 horse was reported as having all 3 signs (Figure 1A). For 6 horses, the cough was recorded as being present only during exercise, while for the other horses, it was either recorded as being present at rest, during rest and exercise, or in broader terms (e.g., “frequent” or “intermittent”). The chronicity of the clinical signs varied from 3 wk to several months. For 4 horses, duration of clinical signs could not be found explicitly in the medical record, but chronicity was assumed based on other information such as other treatments tried before presentation. Twenty-seven horses had an increase in neutrophil percentage in their BALF, 23 horses had increased mast cells, and 10 had increased eosinophils. The different combinations are represented in Figure 1B.

Figure 1.

Clinical signs and bronchoalveolar lavage cytology on presentation. A — Clinical signs of horses on presentation (n = 33). Each horse can have more than one sign. B — Number of asthmatic horses with different combinations of inflammatory cell population above reference range in their bronchoalveolar lavage fluid.

Treatments implemented

All 33 owners reported having implemented dust reduction measures (decreased exposure to barn dust or to hay dust), which included, in all but 1 case, removal of dry hay from the horse’s diet. Despite our recommendations, more than half of the owners (12) elected to use soaked hay (6 of them also used pellets at times). Only 3 used pasteurized hay, and 12 replaced hay completely with a pelleted diet. Among the 17 owners who used soaked hay, 3 reported it was the only management change and the other 14 used it in combination with additional dust reduction measures. Twenty-six horses were turned-out more often than prior to evaluation. Diet change and increased turnouts were temporary (i.e., were no longer in place at the time of questionnaire) for 44% and 26% of horses, respectively (not significantly different, P = 0.18). Also, 30% of owners reported that they had made a rigorous and permanent change in management. Seventeen horses (52%) had received oral or inhaled corticosteroids, and 6 (18%) had received bronchodilators. None of the horses was medicated at the time of the survey.

Short-term outcome

Twenty-one owners (64%) reported a 90% to 100% overall improvement in clinical signs and 3 reported an 80% improvement for a total of 24 owners (73%) reporting a positive outcome, which also corresponds to the overall “satisfaction” reported (74%). Four owners reported a 50% or less improvement and 5 owners reported minimal or no improvement, for a total of 9 (27%) horses classified as having a negative outcome (Figure 2). No deterioration in clinical signs was reported. When horses had more than 1 clinical sign on presentation, improvement was similar (± 5%) for all clinical signs, except for 1 patient with a 90% improvement reported for cough and 0% for nasal discharge and performance. This horse was considered as having a negative outcome due to the persistence of poor performance and nasal discharge. Clinical signs on presentation were not associated with outcome (cough: P = 0.11, poor performance: P = 0.40, nasal discharge: P = 0.21), but horses with a negative outcome were significantly older on average than horses with a positive outcome (Figure 3). No single treatment intervention was significantly associated with improvement in clinical signs, but the proportion of positive outcome tended to be higher when horses spent more time outside (in addition to limiting exposure to dry hay) (Figure 2, 81%, P = 0.07). In our data, bronchoalveolar lavage inflammatory cell type, initial clinical signs, and time since diagnosis were not associated with outcome (Figure 3), neither was breed or gender, but due to the low number of cases, a potential role of these factors cannot be ruled out.

Figure 2.

Short-term outcome reported by owners. A — Overall improvement of horse’s clinical signs, 0% being equivalent to “no improvement” and 100% to “complete resolution of clinical signs.” B — Percentage of positive and negative outcomes with treatment implementation. Horses with a reported 50% overall improvement or less were classified as having a negative outcome. GCs — glucocorticosteroids.

Figure 3.

Horse’s characteristics in relation to outcome. A — Age on presentation of horses with positive (open circles) and negative (black circles) outcome. B — Time since diagnosis for horses with positive (open circles) and negative (black circles) outcome. C — Bronchoalveolar lavage fluid cell types in horses with positive (open circles) and negative (black circles) outcome. D — Initial clinical signs in horses with positive (white bars) and negative (black bars) outcome. N = 22 and 6 for cough, 6 and 4 for poor performance, and 5 and 4 for nasal discharge.

Discussion

Poor adherence to treatment recommendations is a common problem in patients with asthma that leads to suboptimal control of the disease (13). Reasons for poor adherence range from difficulty with administration of medication (mainly for inhalers), incomplete understanding of the treatment strategy, and sometimes conscious decision that the burden of the treatment outweighs the burden of the disease (14). Although there are little data on adherence to treatment programs in equine asthma, these factors may also play a role in the management of the disease. Here, the reported adherence was surprisingly high, as was overall satisfaction. All owners indicated that they had implemented at least 1 of the recommendations to decrease exposure to hay dust or barn dust. However, for 3 horses, it only meant soaking the hay, which is not a typical recommendation in our hospital, for lack of perceived efficacy and contradictory reports on its effect on reducing inhalable dust without reducing live mold and bacteria content (15,16). Of note, these 3 horses were in the “negative outcome” group. Contrary to our hypothesis, adherence to recommendations was greater for dust control measures (including partial and temporary) than for administration of medication (100% versus 55%). This could, in part, result from dust reduction measures, which are most often discussed first, and medication recommended if clinical signs persist despite environmental changes. However, only 30% of owners made changes that were both rigorous and permanent. Interestingly, in this study, 52% of horses with a positive response to treatment eventually returned to dry hay feeding. Unfortunately, the average duration of the changes reported as transient could not be determined. This, combined with the fact that horses with negative outcome were older than horses with a positive outcome, supports the concept that a proportion of young horses with moderate equine asthma are only transiently affected. However, it is also possible that some owners become more tolerant to clinical signs over time, or that the environmental changes we proposed were difficult to implement on a long-term basis (i.e., many years). Moreover, with many of the horses being turned out more often, there is a potential for spurious decline in observed cough. The absence of significant association between outcome and the type of treatment can reflect the lack of standardization in treatment combinations, the subjective evaluation from the owners, and a lack of power due to the small number of horses with poor outcome. Specifically, environmental or dietary changes should not be ruled out as having a potential positive effect on outcome.

The aim of this study was to evaluate the satisfaction of clients after implementation of dust control measures, with or without concurrent medication administration. The main limitations of this study are related to its retrospective nature, the lack of a control group, variability of treatments implemented, and the lack of objective measures of outcome (standardized effort test, respiratory function, and BALF cytology). The order in which owners implemented the different approaches likely depended on practical considerations, and therefore, contributed to the estimation of their efficacy. Since most inhaled dust contributing to equine asthma comes from hay (12,17) and because stabled horses are exposed to much higher concentrations of endotoxin than horses maintained on pasture (up to 8-fold) (18), the relative contribution of dry hay avoidance and barn dust avoidance is difficult to separate, especially when owners tend to implement both measures concurrently. Moreover, in the absence of an untreated group, the proportion of horses that would improve without intervention is unknown and could contribute to an overestimation of the perceived efficacy of some treatments. Also, there have been significant advancements in the management of horses with equine asthma in the past decade. This study was conducted before steamed hay was more commonly used and before the reported additional benefit of adding omega-3 fatty acids to a complete pelleted diet in horses with airway inflammation (19). Also, newer inhaled corticosteroids and bronchodilators were not included in our standard recommendations in 2010–2012. Finally, potential bias includes selective memory of the owner when responding to the questionnaire, as well as memory bias that tends to overestimate the degree of adherence to recommended treatment regimens (20).

In conclusion, application of dust control measures resulted in a substantial perceived improvement in most horses affected with moderate equine asthma. Regardless of the recommendations implemented, close to 75% of owners reported clinical improvement that met their satisfaction. Prospective and standardized studies, including a more reliable monitoring system to detect subtle clinical signs, are needed to evaluate the effect of different treatments on long-term outcome. CVJ