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Keywords:

  • horse;
  • Rhodococcus equi;
  • foal;
  • ecology;
  • air sampling;
  • breath sampling;
  • breathing zone

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

Reasons for performing the study: Disease caused by Rhodococcus equi is a significant burden to the horse breeding industry worldwide. Early detection of rhodococcal pneumonia, albeit important to minimise treatment costs, is difficult because of the insidious nature of the disease and the lack of definitive diagnostic tests.

Objectives: To investigate air sampling from the breathing zone of neonatal foals as a predictor of subsequent rhodococcal pneumonia.

Methods: Air samples were collected from the breathing zone of 53 neonatal foals (age ≤10 days) and again at the time of routine ultrasonographic screening for R. equi pneumonia (age 1–2 months).

Results: Pneumonia was diagnosed ultrasonographically in 23% of foals. Virulent R. equi was detected in air from the breathing zone of 19% of neonatal foals and 45% of foals at age 1–2 months. There was no association between virulent R. equi in the breathing zone of foals and the subsequent ultrasonographic diagnosis of rhodococcal pneumonia. The median concentration of virulent R. equi in the breathing zone of both neonates (0 [range 0–4] colony-forming units [cfu]/250 l) and older foals (0 [range 0–3] cfu/250 l) was not significantly different from that in background air samples (0 [range 0–6] cfu/250 l). There was no difference in the concentration of virulent R. equi in the breathing zone of older foals that were diagnosed with rhodococcal pneumonia or clinically normal foals.

Conclusion: Detection of virulent R. equi in air from the breathing zone was not a positive predictor of rhodococcal pneumonia in foals up to age ≤2 months.

Potential relevance: Selective culture of air samples from the breathing zone of young foals is not better at diagnosing rhodococcal pneumonia than early ultrasonographic screening. However, culture of air samples from the breathing zone of older foals remains a useful herd-based epidemiological tool.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

Rhodococcus equi is a Gram-positive coccobacillus found commonly in soil. R. equi causes pyogranulomatous bronchopneumonia in foals and immunocompromised human patients (Zink et al. 1986; Donisi et al. 1996; Weinstock and Brown 2002). Infection with R. equi can also result in abscess formation in the foal gastrointestinal tract or other parts of the body, although these manifestations of disease are less common than pneumonia (Reuss et al. 2009). Disease caused by R. equi has a significant economic impact on the horse breeding industry worldwide. Costs of treatment and foal losses on farms with endemic disease can be substantial (Pilkington and Wilson 1993; Takai et al. 1995). Early detection of infection with R. equi allows treatment to start before the clinical signs of disease are severe, and this is of great importance in reducing foal wastage and the costs associated with lengthy antimicrobial therapy.

The purpose of this study was to investigate the use of air samples collected from the breathing zone of neonatal foals as a predictor of subsequent development of rhodococcal pneumonia in the same foals in later life. In addition, the contribution of organisms collected from the breathing zone of foals to the overall airborne burden of virulent R. equi was investigated.

Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

Study population

Samples were collected from 53 Thoroughbred foals born during the last 2 weeks of August, the months of September, October, November and the first week of December 2007 on a farm endemically affected by R. equi in New South Wales, Australia. Air samples were collected from the breathing zone of all foals as neonates (aged 2–10 days) and again from the same foals at age 1–2 months, at the time of routine ultrasonographic screening for rhodococcal pneumonia. Blood samples were also collected from foals at the time of routine ultrasonographic thoracic screening at age 1–2 months, for determination of total and differential white blood cell and fibrinogen concentrations. For the purposes of this study, a case of rhodococcal pneumonia was defined as any foal that had ultrasonographic evidence of pulmonary abscessation with or without clinical signs of rhodococcal pneumonia.

Samples collected

Air samples were collected from the breathing zone of the foals by holding a portable microbiological air sampling device (M Air T)1 in front of the nostrils of each foal while it was manually restrained. Each breath sample comprised 250 l of air collected onto a selective agar plate, as previously described (Muscatello et al. 2009). The procedure took approximately 2 min/foal. Between 2 and 6 background environmental air samples of the same volume were taken each month at foal muzzle height from the same sites on the farm using the same equipment. Where possible, background air samples were taken on the same day as foal breathing zone samples, although this was not possible for all monthly sampling periods.

Bacteriology

Selective agar plates (modified CAZ-NB) (von Graevenitz and Punter-Streit 1995; Muscatello et al. 2007) were incubated for 48–72 h at 37°C. Colony blotting and DNA hybridisation were used to identify virulent R. equi and to differentiate between avirulent and virulent isolates in air samples from the breathing zone of foals and environmental air samples, as previously described (Arriaga et al. 2002; Muscatello and Browning 2004; Muscatello et al. 2009).

Ultrasonographic diagnosis of rhodococcal pneumonia

Thoracic ultrasonographic examinations, using a 5 mHz linear probe, were performed on all foals in residence on the farm at age 1–2 months, unless prior examination was indicated by the presence of clinical signs. Ultrasonographic evidence of hypoechoic areas within the superficial lung parenchyma was considered indicative of pulmonary abscessation caused by R. equi.

Data analysis

Data were analysed using Wilcoxon's signed ranks (paired count data), Mann–Whitney U (independent count data) or McNemar's (paired proportions) tests to evaluate clinical and culture data as appropriate, with odds ratios from exact conditional logistic regression (paired proportions) and logistic regression (independent proportions) used to illustrate the strength of significant associations. Statistical analysis was performed using Stata 11.1 for Windows2 and GraphPad InStat version 3.0 for Windows3. P values <0.05 were regarded as significant.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

Prevalence of rhodococcal pneumonia

The prevalence of rhodococcal pneumonia diagnosed by thoracic ultrasonography was 23% (12/53 foals) and the median age of foals at diagnosis was 41.5 days (range 29–57 days). The age at diagnosis was strongly influenced by the timing of the ultrasonographic screening protocol on the farm. Ultrasonographic diagnosis of R. equi pneumonia was associated with clinical signs of disease in only 2 of 12 foals. These 2 foals were observed to be ill thrifty and were heard to cough prior to the age at which routine ultrasonographic screening occurred.

Comparison of virulent R. equi concentrations in exhaled breath of neonatal and 1–2-month-old foals

The proportion of foals that had virulent R. equi detected in air samples from the breathing zone was determined for each of the monthly sampling periods. Virulent R. equi was detected in the breathing zone of 10/53 neonatal foals in the study population (19%; 95% confidence interval [CI] 9–32%) (Table 1). The median concentration of virulent R. equi in air samples from the breathing zone of neonatal foals over the study period was 0 (range 0–4) colony-forming units [cfu]/250 l. Virulent R. equi was detected in the breathing zone of 24/53 foals (45%; 95% CI 32–60%) examined at age 1–2 months. Virulent R. equi was significantly more likely to be detected in the breathing zone of 1–2-month-old foals than from the same foals as neonates (odds ratio [OR] 3.8; exact 95% CI 1.4–13.0; P = 0.007) (Table 1). The median concentration of virulent R. equi in air samples from the breathing zone of 1–2-month-old foals over the study period was 0 (range 0–3) cfu/250 l. The concentration of virulent R. equi detected in air from the breathing zone of 1–2-month-old foals was significantly greater than when they were neonates, when results were compared across the whole study period (P = 0.009).

Table 1. Concentrations of virulent R. equi detected in exhaled breath of neonatal and 1–2-month-old foals and in background air samples
Source of air sampleVirulent R. equi concentration (colony-forming units/250 l)
0123>3
Neonatal foal43 (81.1%)7 (13.2%)2 (3.8%)1 (1.9%)0
1–2-month-old foal29 (54.7%)13 (24.5%)8 (15.1%)3 (5.7%)0
Background air13 (65%)2 (10%)3 (15%)1 (5%)1 (5%)

Association between air samples collected from the breathing zone and diagnosis of rhodococcal pneumonia

There was no significant association between the detection of virulent R. equi in the breathing zone of neonatal foals and the subsequent ultrasonographic detection of lung abscesses in those individuals. Three out of 12 disease-positive foals had virulent R. equi detected in air from the breathing zone as neonates (sensitivity 0.25; 95% CI 0.05–0.57). Thirty-four of 41 disease-negative foals had no virulent R. equi detected in air from the breathing zone as neonates (specificity 0.83; 95% CI 0.68–0.93). Nor was there any significant association between the detection of virulent R. equi in the breathing zone of 1–2-month-old and the diagnosis of rhodococcal pneumonia by thoracic ultrasonography. Five out of 12 disease-positive foals had virulent R. equi detected in air from the breathing zone at age 1–2 months (sensitivity 0.42; 95% CI 0.15–0.72). Twenty-two of 41 disease negative foals had no virulent R. equi detected in air from the breathing zone as 1–2-month-old (specificity 0.54; 95% CI 0.37–0.69).

Despite foals having a significantly lower concentration of virulent R. equi detected in air from the breathing zone when sampled as neonates than when sampled at age 1–2 months, the concentration of virulent R. equi in the breathing zone of foals was not associated with a diagnosis of R. equi pneumonia in either age group. The median concentration of virulent R. equi detected in air from the breathing zone of 41 neonatal foals that had no lesions detectable by ultrasonographic examination (median 0 [range 0–4] cfu/250 l) was not different from the concentration detected in the 12 foals that were subsequently diagnosed ultrasonographically with rhodococcal pneumonia (median 0 [range 0–1] cfu/250 l; P = 0.64). When sampled at age 1–2 months, the concentration of virulent R. equi detected in the breathing zone of those 12 foals diagnosed ultrasonographically with rhodococcal pneumonia (median 0 [range 0–3]) was also not different from that detected in the 41 foals with no detectable lesions (median 0 [range 0–3]) cfu/250 l; P = 0.67).

Concentration of virulent R. equi in background air

Samples of background air were taken in August (n = 3), September (n = 2), October (n = 5), November (n = 5), December 2007 (n = 1) and January 2008 (n = 4) from the same areas of the farm in which foals were sampled (Table 1). Virulent R. equi was detected in 7 out of 20 environmental air samples (35%, 95% CI 15–59%) collected throughout the study period. The median concentration of virulent R. equi in background environmental air samples during the study period was 0 (range 0–6) cfu/250 l. The concentrations of virulent R. equi in air samples from the breathing zone of neonatal and 1–2-month-old foals were not significantly different from those of the surrounding air over the whole study period (P = 0.09 and 0.70, respectively).

Association between diagnosis of rhodococcal pneumonia and haematological tests

Blood samples for haematology and fibrinogen estimations were collected from 52 of the 53 foals in the study population. Foals with an increased white cell count (>12 × 109cells/l) at the time of thoracic ultrasonography were more likely to be diagnosed with rhodococcal pneumonia than foals with normal (6–12 × 109cells/l) white cell counts (OR 7.0; 95% CI 1.6–30.4; P = 0.009). There was no significant association between hyperfibrinogenaemia (>4 g/l) and diagnosis of rhodococcal pneumonia (OR 2.0; 95% CI 0.5–8.0; P = 0.31). However, foals with concurrent elevations of white cell count and fibrinogen concentrations were more likely to be diagnosed with rhodococcal pneumonia than foals with normal white cell counts and fibrinogen levels (OR 7.2; 95% CI 1.3–39.6; P = 0.023).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

Morbidity rates for rhodococcal pneumonia in foals vary between farms and may be influenced by the methods used for diagnosis (Pilkington and Wilson 1993; Chaffin et al. 2003; Venner et al. 2009; J.R. Gilkerson, unpublished data). Early screening methods employed on the farm in this study detected ultrasonographic lesions consistent with pulmonary abscesses caused by R. equi in 23% of the study population, most with no overt signs of respiratory disease. Ultrasonographic screening techniques are more sensitive at diagnosing disease than clinical signs alone (Ramirez et al. 2004), and early diagnosis of rhodococcal pneumonia is an important factor in reducing mortality rates (Prescott et al. 1989; Giguere and Prescott 1997). However, it is recognised that some foals with ultrasonographically detectable pulmonary lesions do not subsequently develop overt clinical signs of disease and thus may have the capacity to overcome subclinical disease without antimicrobial treatment (McCracken and Slovis 2009; J.F. Freestone and C.D. Collins, personal communications). Therefore, on a farm that did not employ early ultrasonographic screening techniques, these foals would potentially remain undetected and estimates of disease prevalence would be lower.

Air sampling has been used in previous epidemiological studies to investigate the contribution of exhaled air to the spread of rhodococcal pneumonia in foal herds and the association between disease incidence and the levels of aerosolised virulent R. equi on Australian stud farms (Muscatello et al. 2006a, 2009). Virulent R. equi was found in significantly higher concentrations in air from the respiratory zone of naturally infected foals than in the background air of high traffic zones on farms (Muscatello et al. 2009). In addition, high levels of aerosolised virulent R. equi on farms were associated with increased disease incidence (Muscatello et al. 2006a). In another recently reported study performed on 2 endemically affected farms in North America, airborne concentrations of virulent R. equi were significantly increased when mares and foals were predominantly housed at the site of air sample collection, either in paddocks or in barn stalls (Kuskie et al. 2011). The current study investigated the detection of virulent R. equi in the breathing zone as a potential diagnostic method for use in individual young foals. It was found to be ineffective as a predictor of rhodococcal pneumonia in individual foals, either as neonates or at age 1–2 months. However, the foals when sampled as neonates had significantly lower concentrations of virulent R. equi detected in the breathing zone than when sampled at age 1–2 months throughout the study period. The open collection system used in this study meant that any sample of air collected from the breathing zone of foals contained a mixture of both exhaled breath and environmental air. The proportion of air collected from the breathing zone of neonatal foals that was attributable to exhaled breath would have been about half that of 1–2-month-old foals owing to the difference in tidal volumes between these 2 groups of foals. The percentage of an air sample collected from the breathing zone of neonatal foals attributable to exhaled breath would only be 25–30%, whereas that from 1–2-month-old foals would be around 50%. Therefore, a high percentage of an air sample from the breathing zone of foals would represent environmental air, particularly in neonates. This reflects a limitation in the study and may explain why there was no difference between virulent R. equi detected in the breathing zone of foals and the background environment. Therefore, this study indicates that air sampling from the breathing zone of foals is more suited to herd-based epidemiological investigations than as a diagnostic test in individuals (Muscatello et al. 2005, 2006a,b; Kuskie et al. 2011). The median concentration of detectable virulent R. equi in the breathing zone samples from both groups was not significantly different from that in the background air samples and therefore reflected the level of environmental exposure of foals to virulent R. equi over the study period. These results were in contrast to a previous study that showed the concentration of virulent R. equi collected from the respiratory zone of foals with naturally acquired R. equi pneumonia to be significantly greater than that in background environmental air of holding pens and laneways on horse farms (Muscatello et al. 2009). Differences in findings between the current study and the previous study may be a result of variation in the age and hence the tidal volume of the foals in the study populations; seasonal differences; differences in location of sample collection and time of sampling; or differences between the farms in the studies.

Recognised routes of R. equi infection in foals are inhalation and/or ingestion (Prescott et al. 1980; Johnson et al. 1983a,b; Yager 1987). Virulent R. equi was detected in the breathing zone of 10/53 (19%) neonatal foals in the study population, supporting the hypothesis that some foals are exposed to virulent R. equi by inhalation of environmental air at a very early age (Horowitz et al. 2001). However, as all foals housed similarly on a particular farm are presumably exposed to a similar environmental burden of aerosolised virulent R. equi, but only a relatively small proportion of foals go on to develop disease, the factors involved in determining whether infection becomes established and subsequently causes disease in an individual foal after exposure to virulent R. equi, are more complex than just exposure to the virulent organism early in life (Cohen 2008; Dawson et al. 2010).

Foals with rhodococcal pneumonia in this study had significantly greater odds of having haematological evidence of leucocytosis, with or without hyperfibrinogenaemia, than clinically normal foals. There was, however, no association between the detection of hyperfibrinogenaemia without concurrent leucocytosis in foals and the ultrasonographic diagnosis of rhodococcal pneumonia. These results support the findings of a recent study in which elevated white cell counts were found to be a useful tool for the early detection of infection with R. equi on a farm with a high prevalence of disease (Giguere et al. 2003), but contrast with a study a number of years ago in which elevated plasma fibrinogen concentrations were detected in all foals diagnosed with rhodococcal pneumonia (Sweeney et al. 1987). The current study found no association between hyperfibrinogenaemia alone and ultrasonographic diagnosis of rhodococcal pneumonia. Foals in the current study were examined on farm and either did not exhibit clinical signs of disease or were diagnosed early in the disease course. In contrast, foals in the study performed by Sweeney et al. (1987) were all hospitalised cases that had a mean duration of clinical signs prior to admission to hospital of 13 days. Hence those cases were more chronically affected and expected to exhibit hyperfibrinogenaemia. Differences between the 2 studies, therefore, may arise from the different diagnostic criteria used to define rhodococcal pneumonia and the different stages of disease at which foals were diagnosed.

The nonspecific nature of the inflammatory response that is measured by changes in white cell count and fibrinogen levels means that detection of haematological changes cannot replace a specific microbiological diagnosis of disease, but the results of this study suggest that haematology may be useful as a screening procedure for rhodococcal pneumonia in instances where thoracic ultrasonography is not an option.

Although the current study showed that virulent R. equi was detectable in air from the breathing zone of neonatal and 1–2-month-old foals, there was no association between the presence of virulent R. equi and ultrasonographic diagnosis of rhodococcal pneumonia. Detection of virulent R. equi in the breathing zone was therefore not a predictor of rhodococcal pneumonia in individual foals aged ≤2 months. The concentration of virulent R. equi in the breathing zone of neonates was low and not significantly different from that in background air samples. Thus there was no indication that virulent R. equi in the breathing zone of neonatal foals increased the overall concentration of airborne virulent R. equi in an area of high environmental burden, although these results were obtained from a relatively small study population on one farm. The concentration of virulent R. equi in the breathing zone of foals at age 1–2 months was also not significantly different from that in the background air over the whole study period, nor was the concentration of virulent R. equi detected in the breathing zone of foals at age 1–2 months different between those diagnosed ultrasonographically with rhodococcal pneumonia and normal foals. In this study, air sampling from the breathing zone was not a particularly specific method for early diagnosis in foals compared to early ultrasonographic screening techniques. These results contrast with previous work (Muscatello et al. 2005, 2009) and suggest that further studies are required to improve our capability to specifically diagnose R. equi infection and implement early therapeutic interventions.

Sources of funding

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

Funding for this research was provided by the Rural Industries Research and Development Corporation (RIRDC).

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

The authors would like to acknowledge the support provided for this study by the stud farm involved, The University of Melbourne, Scone Equine Hospital and the Hunter Valley Equine Research Centre (HVERC).

Manufacturers' addresses

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References

1 Millipore, Saint-Quentin-Yveline, France.

2 StataCorp, College Station, Texas, USA.

3 GraphPad Software, San Diego, California, USA.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conflicts of interest
  8. Sources of funding
  9. Acknowledgements
  10. Manufacturers' addresses
  11. References
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