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- Materials and methods
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Reasons for performing study: Dorsal displacement of the soft palate (DDSP) is one of the most common obstructive conditions of the upper respiratory tract in the racehorse. This condition has a complex aetiology which may be caused or exacerbated by pharyngeal inflammation. Additionally, lower respiratory airway diseases may be associated with DDSP thereby contributing to exercise intolerance in these horses.
Objective: The aim of this study was to measure physiological variables during a standardised exercise test and to assess the prevalence and consequences of lower respiratory airway disease in horses with DDSP.
Methods: A total of 46 horses were included in this study: 22 in the control and 24 in the DDSP groups. All horses performed a SET with measurement of heart rate (HR) and blood lactate concentration. One hour post exercise, respiratory samples were collected for cytological and bacteriological analysis.
Results: During exercise, the DDSP group had higher blood lactate concentration than the control group. According to BAL results, 50 and 63% of control and DDSP group horses, respectively, had evidence of inflammatory airway disease (IAD). In the DDSP group, 42% of horses had a syndrome of tracheal inflammation (STI) with 71% of this group having bacteria isolated at >105 CFU/ml.
Conclusions: Horses with DDSP showed evidence of a high prevalence of IAD and STI with an associated positive bacteriology in 55% of the cases. Even if DDSP is treated by surgery, the authors' recommendation would be to investigate the possibility of lower respiratory airway problems which may also be impacting the horse's performance and/or surgery efficiency.
- Top of page
- Materials and methods
- Conflicts of interest
- Manufacturers' addresses
Dorsal displacement of soft palate (DDSP) is the most common cause of dynamic obstruction identified during treadmill exercise in racehorses (Martin et al. 2000; Lane et al. 2006a). Most affected horses make an abnormal noise during exhalation during a fast work (a ‘snoring’ noise). However, in approximately 30% of horses with DDSP, this noise is not reported (Franklin et al. 2004). In our study, in the DDSP group, 83.3% of the horses were presented with a history of a respiratory noise during exercise which is in accordance with previous studies (Franklin et al. 2004; Lane et al. 2006b). However, we did not record the presence of abnormal noise during high speed treadmill exercise.
Resting endoscopic examination has limited value in determining if a horse will experience DDSP during exercise. Although Holcombe et al. (1996) have reported that clinicians can create negative intrapharyngeal pressures during nasal occlusion, equivalent to negative pressures experienced during high-speed exercise, many horse that displace at rest do not displace during high speed exercise and the reverse is also true (Parente and Martin 1995; Ferrucci et al. 2004; Tan et al. 2005; Lane et al. 2006b). This was the case in this study as only 2 of the 24 horses (8.3%) showed a DDSP during nasal occlusion at rest. Also, it has been suggested in previous reports that some abnormalities observed at rest may point to a diagnosis of DDSP during exercise. These include prolonged spontaneous dorsal displacement, displacement and/or billowing in response to nasal occlusion or swallowing, ulceration of the caudal border of the soft palate and/or the presence of a hypoplastic or flaccid epiglottis. In our study, only one of the 24 horses had ulceration of the caudal border of the soft palate and 2 had a flaccid epiglottis at rest. These 2 horses also demonstrated displacement of the soft palate in response to nasal occlusion. Also, all horses in the DDSP group had a normal length epiglottis as measured on a standardised lateral radiograph of the pharyngeal region according to Linford et al. (2002). The authors suggest that this rules out epiglottic hypoplasia as a cause of DDSP during exercise in these horses. This was already reported by Rehder et al. (1995) who showed that in a population of DDSP horses the epiglottic size was within normal limits.
Considering upper airway inflammation occurrence, there is in racehorses, a high prevalence of pharyngeal lymphoid hyperplasia (PLH). In a population of 1005 Thoroughbred horses, Saulez and Gummow (2009) showed that 63% of the horses had a grade 2–4 PLH, with grades 3 and 4 occuring in younger racehorses. This is in accordance with our study in which 54.2% of the horses also had a grade 2–4 PLH, with young horses showing significantly higher grades of PLH. Age may be a risk factor for DDSP as young horses show higher grades of PLH and as upper airway inflammation may lead to DDSP.
IAD has recently been redefined (Couetil et al. 2007) as a nonseptic inflammation affecting horses of any age with a definitive diagnosis based on BALF cytology. The cytological profile of IAD is characterised by an increase in the total nucleated cell count with mild neutrophilia or alternatively increased mast cell or eosinophil percentages (Couetil et al. 2007).
A distinction has recently been made between IAD and the syndrome of tracheal inflammation (STI) but the relationship between the 2 conditions is unknown. One of the reasons for this distinction may be the poor correlation found between TW and BALF cytology (Malikides et al. 2003; Allen et al. 2006). Therefore, there is a consensus that the best chance of arriving at a correct diagnosis of intermediate and lower respiratory tract inflammation is afforded by performing both TW and BAL (Malikides et al. 2003; Hodgson 2006; Ramzan et al. 2008). In the present study, both TW and BAL were performed and there was a significant difference for the percentages of macrophages, haemosiderophages, mast cells, epithelial cells and neutrophils between TW and BAL.
The differential cell count may be performed on either leucocytes or on nucleated cells which includes epithelial cells (Hewson and Viel 2002). In a recent review on laboratory findings in respiratory fluids, Richard et al. (2009b) presented reference values from various studies for TW and BALF cytology. However, the results are difficult to compare as the methodology varies from one study to the other and presentation of the results differs, some authors including epithelial cells and some not. In order to evaluate the incidence of epithelial cells inclusion or not on other cells percentage (macrophages, haemosiderophages, lymphocytes, neutrophils, eosinophils, mast cells, giant cells), the results in this study were presented with both total nucleated cell count (TNCC) and leucocyte count (LC).
There have been no published accepted values for the different cell types observed in the TW cytology, although it was reported that in young, clinically normal racehorses, the neutrophil count was <20% of the leucocytes in 73–80% of horses examined (Sweeney et al. 1992a; Christley et al. 2001). In the current study, control group horses showed 4.3% (± 2.4) neutrophils as part of the leucocyte count and 3.7% (± 2.3) when considered as part of the total nucleated cell count. Regardless of how results were expressed, all horses in the DDSP group had >20% neutrophils in TW samples. In addition to the differential cell count, the morphological description of the cells may also be informative. This has been shown in a recent study by Fortier et al. (2009) which studied the potential role of BAL and TW in the detection of equine herpesvirus. In BAL, exfoliated epithelial cells and ciliocytophtoria were associated with PCR evidence of EHV-2 and EHV-5 virus-types in the BAL. When examining TW's, the detection of EHVs was correlated with the polymorphonuclear neutrophil count. However, in the current study, no PCR was performed on the respiratory samples. Also, there were no cell abnormalities in the various respiratory samples.
Exercise may also result in changes in BAL and TW cytology, as high speed exercise may lead to a higher number of neutrophils (Couetil and Denicola 1999; Malikides et al. 2007). Therefore, the most convenient time for collection of a tracheal wash sample to obtain the most diagnostically useful information might be after a suitable ‘washout’ period of at least 1–2 h post exercise (Malikides et al. 2007). In our study, respiratory sampling was performed 1 h after a maximal exercise. Also, the amount of neutrophils in a BALF is inversely proportional to the quantity of saline instilled (Sweeney et al. 1992b; Richard et al. 2009b). Instillation of a 120 ml volume may explain the higher neutrophils amount compared to other studies in which saline volumes were more important. In this study, horses in the control group had a neutrophil percentage in the BAL >10%: neutrophils = 11.8% ± 6.4 when considered as a percentage of nucleated cell count and 12.2% ± 6.6 when considered as a percentage of the leucocyte count. This is in accordance with a previous study in which neutrophils percentage for the control group was 15% for a BAL collected under the same conditions (Couroucé-Malblanc et al. 2002). Because of the methodology used (120 ml saline instilled and fluids samples taken 1 h after exercise) and because of these results, our definition of IAD was based on ≥15% neutrophils in the BALF with STI defined as there being ≥20% neutrophils in a TW sample. The neutrophils percentage is expressed as a percentage of leucocyte count.
Tracheal inflammation associated with mucus accumulation is known to have a negative impact on performance (Holcombe et al. 2006). However, in the present study, tracheal endoscopy was performed 1 h after exercise which will have an influence on the presence of mucus and as such the visual tracheal mucus score. This is why no mucus score was ascribed in the present study. However, the authors suggest that a tracheal lavage score as described by Ramzan et al. (2008) may have been utilised in an attempt to better differentiate horses according to the variation in mucus characteristics (e.g. accumulation, viscoelasticity).
Exercise-induced pulmonary haemorrhage (EIPH) was defined according to the definition adapted from Newton and Wood (2002). This involved a cytological diagnosis based on examination of BALF in which >20% of macrophages were haemosiderophages. In the current study, 26.7% of horses in the DDSP group with IAD had EIPH. In contrast, no horses in the control group had EIPH as defined by Newton and Wood (2002). However, free red cells were found in the BALF of all horses thus leading to the suspicion of some form of recent pulmonary haemorrhage in these animals.
Care should be taken when interpreting bacterial cultures taken from the intermediate or lower respiratory tract. Since many bacteria detected also belong to the commensal flora of the upper airways (Robinson and Derksen 1998), isolation of bacteria in TW may represent infection, transient intermediate airway colonisation or contamination of the sample. A comparison of percutaneous (transtracheal) aspiration and transendoscopic tracheal wash using a guarded sterile catheter, as used in this study, found no significant difference between both techniques with respect to sample contamination (Christley et al. 1999). In a longitudinal study performed over 3 years in Thoroughbreds, 22% of the TW samples had no bacteriological growth (Wood et al. 2005). This is similar to the current study in which 27% of the horses had no bacteriological growth. Isolation of bacteria from TW samples has previously been associated with lower airway inflammation in racehorses (Chapman et al. 2000; Christley et al. 2001; Wood et al. 2005). The chances of airway inflammation being present are significantly greater with increased numbers (CFU/ml) of Streptococcus zooepidemicus (Burrell et al. 1996; Wood et al. 2005) and Actinobacillus spp. (Wood et al. 2005). However, only TW and not BAL was performed in these earlier studies. Therefore, there may be a relationship between tracheal infection and STI but not between tracheal infection and IAD (Couetil et al. 2007). In the current study, 66.7% of horses with DDSP had evidence of intermediate and/or lower respiratory tract disease with 44–59% of them having STI (8.3% had only STI with 91.7% having STI and IAD) and 62.9% with IAD. For horses with evidence of STI, 75% of them had a positive bacteriological culture with bacteria isolated ≥105 CFU/ml. This is in accordance with a previous study showing 80% prevalence of IAD in horses with ≥105 CFU bacteria/ml isolated (Wood et al. 2005) and with the hypothesis that aerobic bacteria are significantly associated with lower airway inflammation. However, other workers suggest caution in interpreting these results because inflammation of the tracheobronchial tree for any reason may leave it more susceptible to colonisation by oropharyngeal bacteria. These bacteria may, therefore, be a consequence of lower airway inflammation, rather than its cause. Nonetheless, because they are potential pathogens, it is likely that they may contribute to the worsening and prolongation of IAD. However, there was also a high prevalence of IAD in the control group (50%). These horses had no STI and when there was bacteriological growth this occurred at <105 CFU/ml. From these results, we suggest that even if there was a high prevalence of IAD in both groups, there was a higher prevalence of STI and a higher number of bacteria isolated from horses with DDSP compared to controls.
Various authors have shown that respiratory abnormalities can limit oxygen exchange (Persson 1983; Morris 1991; Persson and Lindberg 1991; King et al. 1994; Couroucé-Malblanc et al. 2002). DDSP is considered a common cause of poor performance in racehorses. It leads to an expiratory obstruction that subsequently results in decreased ventilation, hypoxaemia and exercise intolerance (Rehder et al. 1995; Holcombe et al. 1998). IAD is frequently diagnosed as a cause of poor exercise performance. However, the true effect of IAD on performance is incompletely documented. Many horses undergoing investigation for poor performance have signs of IAD. However, given the high prevalence of IAD, the clinical relevance of this finding remains uncertain. Nyman (2003) failed to identify an obvious difference in IAD-affected horses, compared to healthy horses, with regard to arterial blood gas changes. In contrast, others have found that in horses with IAD, gas exchange is impaired during exercise these horses exhibiting worsening of exercise-induced hypoxaemia (Couetil and Denicola 1999; Couroucé-Malblanc et al. 2002; Sanchez et al. 2005). Furthermore, it has been shown that IAD horses have evidence of a degree of airway obstruction (Couetil et al. 2001). Post exercise, horses with IAD have higher blood lactate concentration than control horses (Couetil and Denicola 1999). Hence, there is experimental evidence that IAD induces physiological changes in exercising horses that may have a negative impact on performance. In this study, horses with DDSP had a higher blood lactate concentration for step 4 which was performed at maximal velocity compared to control horses. This appears to be in accordance with the occurrence of DDSP which happens more frequently at the end of a maximal exercise such a race. Interestingly, the authors found that horses with DDSP and IAD and also DDSP, IAD and EIPH showed higher blood lactate concentration and thus lower V4 values compared to control. This was not the case with horses with DDSP only. It has been previously shown that V4 may be assimilated to the aerobic capacity of the horse and is significantly related to race performance in the horse and particularly in trotters (Leleu et al. 2005). Therefore, we suggest that horses with both DDSP and lower respiratory diseases such as IAD with or without EIPH are more exercise intolerant at submaximal and maximal exercise intensity.
In the present study, 4 horses showed subclinical locomotor diseases (lameness) and 2 showed a grade 2 right sided holosystolic murmur which was, in both cases, a murmur consistent with tricuspid regurgitation which is frequent in racehorses and seldom associated with poor performance (Young et al. 2008). This underlines the fact that poor performers may have several concomitant problems. Horses with evidence of upper respiratory disease may show concurrent lower respiratory tract disease (STI and/or IAD and/or EIPH) with or without bacterial isolation and other problems such as cardiac and/or muscular and/or locomotor problems (Martin et al. 2000; Couroucé-Malblanc et al. 2002; Richard et al. 2009b). Therefore, we recommend that a thorough and careful examination of the horse is of great importance in horses with poor performance, especially as in this series where we studied DDSP. Tack modifications such as the use of a bit that maintains the position of the tongue, tongue-ties and the figure-of-eight noseband are traditional approaches that may be of value in reducing the occurrence of DDSP (Franklin et al. 2002; Barakzai and Dixon 2005). Also, the treatment of any concurrent diseases may be necessary before undertaking surgical treatment for DDSP. We suggest that in any horse, with or without upper airway dysfunction, that has evidence of active upper, intermediate or lower respiratory airway inflammation, the initial therapy should focus on decreasing this inflammation by medical therapy. Also, as seen previously, presence of bacterial colony may be associated with STI and IAD. Because they are potential pathogens, it is likely that they may contribute to the worsening and prolongation of lower airway inflammation. Therefore, in these cases, it seems important to have an antibiotic medical therapy associated with corticosteroids to decrease inflammation. If the horse suffers from a subclinical locomotor disease, it is also important to undertake a thorough orthopaedic evaluation and to treat the horse as some anectodal reports indicate that the associated pain is considered to be the key factor leading to DDSP. In support of this premise, 2 of the horses in this study with locomotor disease received treatment for their orthopaedic problem and thereafter did not have occurrence of DDSP.
In conclusion, this study demonstrated that exercise intolerance in horses with DDSP may be exacerbated by concomitant underlying lower respiratory tract problems such as STI with or without the presence of bacteria in the trachea and/or IAD and/or EIPH. Our study also showed that a high prevalence of IAD occur in horses performing well (control group). However, these controls animals had no evidence of STI and, when they had bacteria in the TW, they were isolated at numbers of <105 CFU/ml. In contrast, horses with DDSP had a high prevalence of STI with 75% of the cases having bacteria isolated at ≥105 CFU/ml. These horses also had a high prevalence of IAD with 23.5% of these cases having EIPH. As DDSP is a complex disease with various possible causes, a careful examination at rest, during exercise and after exercise should be done on horses thought to have this disease. According to follow-up of the horses in this study and as poor performance may have a number of various components, we recommend that this examination should include endoscopy before, during and after exercise with evaluation of upper respiratory airway at rest (response to nasal occlusion) and during exercise and by scoring the degree of pharyngitis and tracheal mucus. It should also include tracheal wash after exercise (with tracheal lavage score and bacteriology and cytology analysis) and bronchoalveolar lavage after exercise (for cytological analysis). If any inflammation of upper and/or lower respiratory airway exists, medical treatment of this is recommended before scheduling attempted a surgical correction of DDSP. Also, even if respiratory problems appear to be the most important problem, a careful evaluation of cardiac, muscular and locomotor systems should be performed with adequate treatment afforded especially in cases of orthopaedic disease.