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Relative Flow-Time Relationships in Single Breaths Recorded After Treadmill Exercise in Thoroughbred Horses
REFEREED
ORIGINAL RESEARCH Relative Flow-Time Relationships in Single Breaths Recorded After Treadmill Exercise in Thoroughbred Horses K. Kusano, DVM,a R.A. Curtis, BSc SMIEEE,b C.A. Goldman, BScAgr,b and D.L. Evans, BVSc, PhDb ABSTRACT Analysis of individual breaths after exercise has potential for pulmonary function testing. The aims of this study were to investigate the dependence of measurements of pulmonary function in single breaths on time postexercise and tidal volume (VT) after treadmill exercise. Five Thoroughbred horses without evidence of airway disease were used. Horses had been previously acclimated to treadmill exercise and to wearing a face mask. A Quadflow spirometer recorded airflow rates continuously during 90 seconds after intense treadmill exercise to fatigue. Indices of function were based on ratios of times within each breath and analyses of the shape of relative flow–time curves within inspiration and expiration. Restricted maximum likelihood, general linear regression, repeated-measures one-way analysis of variance (ANOVA), and two sample t-tests were used, with statistical significance at P < .05. Time postexercise had no effect on several ratios based on time for inspiration (TI) and expiration (TE), and times to peak flows (TI/TT, TE/TT, TE/TI, Tpef [peak expiratory flow]/ TE, and Tpif [peak inspiratory flow]/TI). Many variables were significantly dependent on VT. Occasional big respiratory cycles with VT more than 10% greater than in the previous breath had significantly different means for relative flow (Rf)/(TE/TI), epz50% (50% of the time from Tpef to end of expiration), epz75% (75% of the time from Tpef to end of expiration), and ipz75% (75% of the time from Tpif to end of inspiration). Predicted means for these variables differed by 10–20%. This study establishes guidelines for the selection of breaths after exercise, and describes a new approach to measurement of relative flow and time relationships. It was concluded that several time-based ratios have potential for measuring pulmonary function. However,
From the Equine Department JRA, Tokyo, Japana; and the Faculty of Veterinary Science, The University of Sydney, New South Wales, Australia.b Reprint requests: R.A. Curtis, 4 Parkes St, Wentworth Falls, New South Wales, Australia. 0737-0806/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jevs.2007.06.005
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care is needed when selecting breaths for calculation of most of the new relative flow–time variables. Keywords: Respiratory; Physiology; Pulmonary; Breathing; Exercise
INTRODUCTION Respiratory tract disease is a common cause of poor performance in racing Thoroughbreds. Upper respiratory tract (URT) disorders have been identified as a contributor to suboptimal racing performance in 8.1%1 and 8.6%2 of horses. Inflammatory airway disease (IAD) is a more common cause of poor performance, interruption of training, and premature retirement in racehorses.3,4 In a population of young racehorses, the prevalence of IAD was 13.8% and the incidence was 8.9 cases/100 horses/month. Diagnosis of respiratory problems relies greatly on endoscopy at rest and during a high-speed treadmill examination5-7 and cytologic examinations.8 Diagnosis of respiratory limitation to performance does not usually include an assessment of limits to breathing, and therefore the degree of limitation to inspiration and expiration are not routinely quantified. In pulmonary function testing (PFT) of humans with suspected lower airway problems, the measurement of peak expiratory flow (PEF) rates and expired air volume in 1 second of a maximal, forced maneuver is commonly used. Maneuver techniques are, however, unsuitable for use in human infants and animals because cooperative compliance to the technique is not possible.9 Therefore, alternative methods also are required to quantify limits to breathing in racehorses. Findings in several studies encourage more research into development of indices of pulmonary function based on measurements in breath-by-breath spirometry during exercise.10-15 Development of techniques for assessment of pulmonary function based on measurements after exercise could increase the applicability of this approach in routine equine veterinary practice. Potentially, suitable measurements could diagnose limits to inspiration or expiration in different respiratory syndromes, assess the severity of a disease, and enable monitoring of responses to treatments. The PFT tests developed must be sensitive and accurate enough to detect subtle changes in respiratory Journal of Equine Veterinary Science Vol 27, No 8 (2007)
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function16 and to enable the differentiation of upper from lower airway breathing limitation. Curtis et al17 described different breath types during and after intense exercise on a treadmill. It was concluded that large breaths, or ‘‘big respiratory cycles’’ (BRCs), were a normal feature of pulmonary ventilation during and after intense exercise. These BRCs may not have the same relative time–flow shapes as the more usual, ‘‘normal’’ breaths, and care should be taken when selecting breaths recorded after exercise for analysis of pulmonary function. Padilla et al18 reported that postexercise hyperventilation in horses resulted in higher tidal volumes in the initial 13-second period of recovery. Tidal volumes within 30 seconds after exercise were similar to or greater than those recorded during prior intense treadmill exercise.17,18 Breaths after exercise may therefore be useful in pulmonary function tests because the lungs are functioning at tidal volumes similar to or greater than those found during intense exercise. Factors that influence the flow, time, and volume relationships in breaths after exercise should be studied to better understand their potential use in equine pulmonary function testing. Development of suitable indices of pulmonary function based on analyses of postexercise breaths could increase the applicability of this approach in veterinary practices. The following questions were addressed in this study: 1. How do measurements of pulmonary function in individual breaths depend on time after intense exercise? 2. Do measurements in BRCs after exercise differ from those in ‘‘normal’’ breaths? 3. Do measurements depend on tidal volume relative to body mass? This paper also describes a new approach to the evaluation of inspiration and expiration in a single breath, using relative flow–time relationships. This approach may obviate the need for production of maximal, forced inspirations or expirations to make a diagnosis if the shape of these relative flow–time relationships in single breaths after exercise depends on the health of the airways.
MATERIALS AND METHODS Five Thoroughbred horses were used in the study (2 male, 3 female; 3–8 years of age and mean body weight 483 kg 13 [SD]). All horses were acclimated to treadmill exercise, to wearing a face mask, and to exercise test protocols. The horses had been in regular treadmill training for 8 weeks before these tests of 5 days per week at speeds of 7–12 m/second. Horses were selected on the basis of tractability and absence of cardiac murmurs. They had no evidence of upper airway abnormalities during treadmill exercise at 12 m/second. No horses had lower airway disease based on tracheal wash results. Further details have been published.19 The experiments were approved by the Animal Use Committee of the Japan Racing Association. The Quadflow spirometer has been described previously.19 The flow sensors measured gas flow to 0.1 L/
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second resolution continuously every 10 milliseconds. Oxygen uptake was not calculated. The barometric pressure, ambient temperature, and relative humidity were recorded before each calibration of flows in left and right sensors. Airflow rates were recorded continuously during 90 seconds after intense treadmill exercise to fatigue. The exercise test consisted of stepped increases in treadmill speed until the horse was no longer able to maintain the same speed as the treadmill. Details of the treadmill exercise test protocol have been described.19 Measurements The Quadflow software measured inspiratory and expiratory flow (L/second) at 100 Hz, and a thermistor measured gas temperature at the nostrils. Barometric pressure, ambient temperature, and humidity were measured in the laboratory before each exercise test. The flow rates were corrected to body temperature and pressure, saturated with water vapor (BTPS). Tidal volume (VT), minute ventilation, and inspiratory and expiratory periods (TI, TE [seconds]) were calculated. Reliability of these measurements within and between horses using Quadflow hardware and software has been described.19 Three consecutive normal breaths were selected in each of the nine 10-second periods in the period immediately after exercise. A group of three breaths was selected from the last three breaths of each 10-second period, unless there was a BRC in that group. A BRC after exercise was defined as a breath having a tidal volume 10% greater than the previous breath.17 If a BRC occurred in the last 3 breaths of a time period, the previous three consecutive normal breaths within the period were selected for analysis. Means of several variables were calculated for each 10-second period (Table 1). The first of the three breaths was used to calculate the variables in Table 2. The parameter ezp25% refers to the percentage of the PEF at 25% of the time from commencement of expiration to the time at PEF (Tpef). Relative flows were also calculated for 50% and 75% of those relative times, and were expressed as ezp25%, ezp50%, and ezp75%. Similar relative flow-time measurements were made for 25%, 50%, and 75% of the time from Tpef to end of expiration (epz25%, epz50%, and epz75%). The same zp% and pz% measurements were made for the next inspiratory phase of the breath (izp25%, izp50%, izp75% and ipz25%, ipz50%, ipz75%). Each BRC in the second to the ninth 10-second interval was identified and the same variables were calculated for those breaths. Statistics Tidal volumes were expressed relative to body mass to help reduce that effect on the values. Restricted maximum likelihood (REML) analyses were used to determine whether significant differences existed between normal and large breaths. General linear regressions were conducted to determine whether measurements were dependent on tidal
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Table 1. Variables measured using mean values of 3 consecutive breaths in each 10-second period
Table 2. Relative flow-time variables calculated in one breath in each 10-second period
Name of Variable
Abbreviation
Description of Measurement
Abbreviations
Respiratory frequency Inspiratory period Expiratory period Time to peak inspiratory flow Time to peak expiratory flow Ratio of inspiratory time to total breath time Ratio of expiratory time to total breath time Ratio of time for expiration to time for inspiration Ratio of time to peak expiratory flow to expiratory time Ratio of time to peak inspiratory flow to inspiratory time Ratio of respiratory frequency to the ratio of TE/TI Peak inspiratory flow Peak expiratory flow Minute ventilation Tidal volume Inspired volume
Rf TI TE Tpif Tpef TI/TT
Percentage of PIF during the period of inspiration from zero flow to PIF Percentage of PIF at 25%, 50%, and 75% of the time taken to attain PIF Percentage of PIF during the period of inspiration from PIF to zero flow Percentage of decrease in PIF at 25%, 50%, and 75% of the time taken to decrease the PIF to zero flow rate Percentage of PEF during the period of expiration from zero flow to PEF Percentage of PEF at 25%, 50%, and 75% of the time taken to attain PEF Percentage of PEF during the period of expiration from PEF to zero flow Percentage of decrease in PEF at 25%, 50%, and 75% of the time taken to decrease the PEF to zero flow rate
izp
TE/TT TE/TI Tpef/Te Tpif/Ti Rf/(TE/TI) PIF PEF VE VT VTI
volumes. Repeated-measures one-way analyses of variance (ANOVA) were used to investigate whether there were significant effects of time postexercise. ANOVA and two-sample t-tests were performed using Sigma Stat 3.5, and all other analyses were performed using GenStat 8th edition. Statistical significance was set at P < .05.
RESULTS Tables 3 and 4 present the means ( SD) of the absolute and relative measurements in breaths studied in the nine 10-second time periods after exercise. Time postexercise had a significant effect on flow and tidal volume after exercise. Time periods 7, 8, and 9 were different (P < 0.05) from time period 1 for all variables. Variables TI, TE, and VTI were not different from each other for time periods 1 to 6. Time postexercise had no significant effect on TI/TT, TE/TT, TE/TI, Tpef/TE, and Tpif/TI. Figure 1 (A and B) shows typical relationships between relative times and percentages of PEF (ezp% and epz%) for expiration in a single breath recorded within 20 seconds after end of exercise. The PEF in this phase of the breath was 75 L/second, and TE was 468 milliseconds. Figure 2 (A and B) shows typical relationships between relative times and percentages of PIF (izp% and ipz%) for the next inspiration in the same breath described in Figure 1. The PIF in this phase was 52 L/second, and TI was 458 milliseconds. Table 5 presents the means (SD) of the epz% and ezp% relative flow rates at 25%, 50%, and 75% of the Tpef. No effects of time postexercise were seen on any variable in
izp25%, izp50%, izp75%
ipz
ipz25%, ipz50%, ipz75%
ezp
ezp25%, ezp50%, ezp75% epz
epz25%, epz50%, epz75%
Abbreviations: PEF, peak expiratory flow rate; PIF, peak inspiratory flow rate.
Table 5. Table 6 provides the means (SD) of the percentages of the izp% and ipz% relative flow rates at 25%, 50%, and 75% of the time taken to increase to peak flow, and the percentages of the decrease in peak flow at 25%, 50%, and 75% of the Tpif. Means for ipz50% in time periods 4, 5, and 7 were greater than in time period 1. Time postexercise had no effect on the other variables in Table 6. Many variables were dependent on tidal volume during recovery, including most of the pz% and zp% relative flow–time variables. BRCs had significantly different means for Rf/(TE/TI), epz50%, epz75%, and ipz75%. Predicted means for these variables in BRCs differed by 10–20% from normal breaths.
DISCUSSION This paper describes a new approach to evaluation of the inspiration and expiration in a single breath, using relative flow–time relationships, and reports on the influence of time postexercise and tidal volume after exercise on the measurements. An ideal measurement would be independent of time and tidal volume after exercise. Only two measurements, izp75% and Tpef/TE, met those criteria. These
Time Period 1
2
3
4
5
6
7
8
9
a
a
TI 0.459 0.092 0.439 0.089 0.426 0.099 0.417 0.099 0.379 0.084 0.360 0.071 0.342 0.076 0.334 0.067 0.336 0.038a TE 0.405 0.077 0.390 0.078 0.405 0.097 0.376 0.089 0.354 0.075 0.347 0.062 0.318 0.058a 0.316 0.059a,c 0.306 0.045 a,c a a,b a,b a,b a,b,c a,b,c,d a,b,c,d VT 25.2 4.05 22.1 4.35 18.9 3.14 17.5 3.10 16.0 2.82 15.5 2.04 13.6 2.03 13.3 2.21 12.4 1.77a,b,c,d VTI 21.8 2.82 19.3 2.63 16.5 1.64 15.3 2.15 13.5 2.15 12.7 1.83 11.2 1.27 a,b 11.1 1.17 a,b 10.9 1.18 a,b a a,b a,b a,b a,b a,b,c a,b PEF 80.8 6.95 74.3 4.77 66.3 6.39 64.8 6.26 64.1 6.07 62.7 5.84 60.1 6.89 61.5 5.02 59.7 4.32a,b,c PIF 68.1 4.47 60.7 6.21a,b 54.4 5.99a,b 50.4 6.54a,b 48.7 5.91a,b,c 48.5 6.77a,b,c 45.1 8.30a,b,c,d 46.2 5.46a,b,c 44.6 5.36a,b,c,d a a,b,c a,b,c a,b,c,d a,b,c,d Rf 72.0 15.26 75.5 16.84 76.0 17.88 79.7 19.36 85.6 20.03 87.5 17.04 93.9 18.75 95.1 18.13 95.3 11.78 a,b,c,d VE 1762.9 137.33 1594.6 134.30a 1370.9 179.33a,b 1356.8 147.95a,b 1310.4 160.00a,b 1322.8 165.98a,b 1261.6 192.29a,b 1242.1 159.88a,b 1176.2 141.11a,b,c,d Abbreviations: TI, inspiratory time (seconds); TE, expiratory time (seconds); VT, tidal volume (L, BTPS); VTI, inspired volume (L,BTPS); PEF, peak expiratory flow (L/second, BTPS); PIF, peak inspiratory flow (L/second, BTPS); Rf, respiratory frequency (breaths/minute); VE, minute ventilation (L/minute, BTPS). a Different from time period 1 (P < .05). b Different from time period 2 (P < .05). c Different from time period 3 (P < .05). d Different from time period 4 (P < .05).
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Table 3. Mean ( SD) of absolute measurements in breaths studies in nine 10-second time periods after exercise
Table 4. Mean ( SD) of relative measurements in nine 10-second time periods after exercise Time Period TI/TT TE/TT TE/TI Tpef/Te Tpif/Ti Rf/(TE/TI)
1
2
3
4
5
6
7
8
9
0.532 0.020 0.468 0.020 0.877 0.076 0.399 0.135 0.271 0.102 82.8 21.04
0.529 0.026 0.471 0.026 0.887 0.102 0.368 0.105 0.379 0.157 87.4 26.46
0.515 0.023 0.485 0.023 0.948 0.108 0.502 0.154 0.302 0.181 82.7 28.41
0.523 0.022 0.477 0.022 0.907 0.093 0.499 0.139 0.340 0.201 92.8 30.09
0.519 0.018 0.481 0.018 0.925 0.073 0.468 0.134 0.345 0.137 94.9 21.92
0.512 0.013 0.488 0.013 0.953 0.047 0.347 0.109 0.295 0.103 94.1 15.15
0.516 0.011 0.484 0.011 0.939 0.043 0.577 0.312 0.346 0.137 99.6 16.97a,c
0.513 0.009 0.487 0.009 0.950 0.035 0.452 0.150 0.396 0.184 100.1 18.35a,c
0.521 0.024 0.479 0.024 0.912 0.105 0.370 0.122 0.392 0.180 106.4 23.73a,b,c
Abbreviations: TI/TT, ratio of inspiratory time to breath duration; TE/TT, ratio of expiratory time to breath duration; TE/TI, ratio of time for expiration to time for inspiration; Tpef/Te, ratio of peak expiratory flow to expiratory time; Tpif/Ti, ratio of peak inspiratory flow to inspiratory time; Rf/(TE/TI), ratio of respiratory frequency to the ratio of TE/TI. a Different from time period 1 (P < .05). b Different from time period 2 (P < .05). c Different from time period 3 (P < .05).
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Figure 1. Relationship between relative time and percentage of peak flow rates for expiration (ezp%, epz%) in a single breath recorded within 20 seconds after end of exercise. A represents relative time and flows from zero flow to peak expiratory flow rate, and B represents relative time and flow rate from peak expiratory flow rate to zero flow rate.
Figure 2. Relationship between relative time and percentage of peak flow rates for inspiration (izp%, ipz%) in a single breath recorded within 20 seconds after end of exercise. A represents relative time and flows from zero flow to peak inspiratory flow rate, and B represents relative time and flow rate from peak inspiratory flow rate to zero flow rate.
results are a new contribution to knowledge concerning evaluation of pulmonary function in horses. The results provide guidance concerning selection of breaths after intense exercise for analysis of pulmonary function. They also provide guidelines for breath selection after exercise in future studies of relative flow–time relationships in studies that investigate the effects of various respiratory problems. Care is needed when selecting breaths after exercise because measurements were dependent on tidal volume and were different in BRCs. Pulmonary function tests based on analyses of postexercise breaths will need to consider both the absolute and relative measurements in conjunction, except for izp75% and Tpef/TE. The relevance of these two measurements to pulmonary function testing is not yet known, and further studies are required in more normal horses and horses with pulmonary dysfunction. Interestingly, the Tpef/TE ratio has recently been used to describe pulmonary function in human infants during normal quiet breathing.20 The basis for selecting breaths immediately after exercise was an expectation that tidal volumes would be greater than during exercise. As a consequence, the lungs would be functioning at closer to a vital capacity after exercise than during exercise. In the first 30 seconds after exercise, mean minute ventilation ranged from approximately
1,400–1,750 L/minute. Art and Lekeux21 reported minute ventilations in Thoroughbred horses during treadmill exercise at 9 m/second of 1,650–1,850 L/minute, with tidal volumes of 14–16 L. Butler et al22 reported similar values during treadmill exercise, and Ho¨rnicke et al13 reported tidal volumes of 10–13 L during maximal field exercise, with PEF and PIF of 67–76 and 56–68 L/second, respectively. Minute ventilations of over 2,000 L/minute were recorded during treadmill exercise at 10 m/second in a group of six horses.17 Those results included data obtained from five of the horses that were used in this study. Tidal volumes in the first 60 seconds after the completion of exercise in the current study were similar to or greater than previously reported values during exercise. These results confirm the potential for use of individual breaths during recovery after exercise for pulmonary function tests in horses. However, PEF and PIF were lower than measured during exercise in other studies. Couetil et al23 have estimated that vital capacities are greater than 40 L in large horses, and therefore it is unlikely that vital capacities would be approached, even during maximal ventilation in the 13-second period after intense exercise. A forced expiratory flow pulmonary function test has been used in resting horses to quantify limits to expiration in resting horses with IAD and chronic obstructive
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Table 5. Mean ( SD) percentages of peak flow rate at 25%, 50%, and 75% of time taken to increase flow to PEF (ezp25%, ezp50%, ezp75%), and percentages of the decrease in PEF at 25%, 50%, and 75% of time taken to decrease flow from PEF to zero flow rate (epz25%, epz50%, epz75%) % of PEF at 3 Relative Times to Attain PEF
% of PEF at 3 Relative Times to Decrease to 0 L/s
Time period
ezp25%
ezp50%
ezp75%
epz25%
epz50%
epz75%
1 2 3 4 5 6 7 8 9
0.56 0.141 0.54 0.175 0.66 0.210 0.60 0.222 0.55 0.123 0.44 0.143 0.58 0.183 0.52 0.083 0.41 0.122
0.86 0.090 0.84 0.111 0.89 0.110 0.87 0.114 0.85 0.068 0.79 0.111 0.87 0.096 0.85 0.070 0.74 0.146
0.96 0.029 0.95 0.046 0.96 0.017 0.95 0.026 0.94 0.024 0.95 0.016 0.95 0.014 0.96 0.019 0.92 0.094
0.92 0.030 0.94 0.024 0.91 0.061 0.93 0.051 0.92 0.017 0.88 0.053 0.90 0.108 0.92 0.036 0.89 0.069
0.77 0.120 0.86 0.089 0.74 0.081 0.80 0.088 0.74 0.056 0.73 0.097 0.75 0.068 0.74 0.121 0.70 0.165
0.62 0.235 0.61 0.169 0.49 0.155 0.49 0.120 0.46 0.152 0.54 0.144 0.49 0.070 0.46 0.185 0.47 0.140
pulmonary disease.23 The studies of expiratory flow curves in IAD cases had greater accuracy and sensitivity for diagnosis than tests using standard pulmonary mechanics. The challenge now is to ascertain whether accurate and sensitive measurements of pulmonary function can be made with analyses in breaths after exercise with tidal volumes that are likely to be less than 50% of vital capacity. To expect that measurements would be most useful in breaths in the first 13 seconds after intense exercise when tidal volumes will be greatest is logical.17,18 However, the mask would probably have to be worn by the horse during prior exercise to satisfactorily record those breaths. The findings by Couetil et al23 encourage further research into techniques for pulmonary function testing that evaluate respiratory air flow at submaximal tidal volumes. Time postexercise had no effect on many fractional time and relative flow–time variables (including TI/TT, TE/TT, TE/TI, Tpef/Te, Tpif/Ti, ezp25%, ezp50%, ezp75%, izp25%, izp50%, izp75%, epz25%, epz50%, epz75%, ipz25%, and ipz75%). For these variables, the Quadflow mask can be applied any time during the 90-second period after exercise. However, there was an effect of time postexercise for ipz50%. The importance of this measurement is yet to be
elucidated, but it could be an important index of limit to breathing during late inspiration. Application of the mask and recording breaths in the first 30 seconds would be desirable for measurements of ipz50%. To measure this variable, one must apply the mask as quickly as possible, or apply the mask before exercise. Significant differences were seen between all other variables over time postexercise. Therefore, comparisons between and within horses cannot be based on selection of breaths at random. A superior approach could be to express the relative time–flow measurements in relation to an absolute measurement in the same breath, such as tidal volume, PEF, or PIF. For example, future research could investigate whether the relationships between the relative flow–time measurements and the peak flow rate for the same breath are different in horses with respiratory problems. Such an approach has a precedent.15 Pulmonary function was described with individual breath analyses during lunging exercise in three groups of riding horses. Regressions of respiratory frequency on relative time ratios (TE/TI) were presented for normal horses and horses with bronchitis and pulmonary emphysema. This paper also referred to ‘‘position’’ of the PIF and PEF within the phase of the breath.
Table 6. Mean ( SD) percentages of peak flow rate at 25%, 50%, and 75% of time taken to increase flow to PIF (izp25%, izp50%, izp75%), and percentages of the decrease in PIF at 25%, 50%, and 75% of time taken to decrease flow from PIF to zero flow rate (ipz25%, ipz50%, ipz75%) % of PIF at 3 Relative Times to Attain PIF
% of PIF at 3 Relative Times to Decrease to 0 L/s
Time period
izp25%
izp50%
izp75%
ipz25%
ipz50%
ipz75%
1 2 3 4 5 6 7 8 9
0.46 0.088 0.57 0.065 0.42 0.097 0.48 0.139 0.51 0.163 0.41 0.111 0.45 0.169 0.47 0.078 0.49 0.098
0.80 0.050 0.93 0.106 0.76 0.076 0.80 0.085 0.82 0.106 0.76 0.086 0.79 0.112 0.79 0.050 0.80 0.059
0.96 0.014 0.97 0.012 0.95 0.024 0.95 0.026 0.96 0.022 0.94 0.034 0.96 0.023 0.93 0.034 0.95 0.033
0.86 0.064 0.91 0.054 0.90 0.076 0.94 0.058 0.92 0.040 0.88 0.086 0.92 0.051 0.92 0.090 0.93 0.052
0.73 0.069 0.79 0.062 0.81 0.068 0.86 0.062a 0.84 0.039a 0.82 0.064 0.84 0.038a 0.83 0.059 0.81 0.059
0.53 0.147 0.64 0.137 0.56 0.108 0.61 0.085 0.67 0.119 0.64 0.098 0.62 0.102 0.63 0.141 0.59 0.097
a
Different from time period 1 (P < .05).
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In our results, we present these ‘‘position’’ values as Tpef/ TE, and Tpif/TI. In Pollmann and Ho¨rnicke,15 the results suggested that Tpef/TE ratios might be lower in the more diseased horses. This finding could reflect a limit to flow in the early phase of expiration. Future studies could use the relative ezp% measurements to quantify relative flow in this phase of the breath with regressions on PEF or tidal volume, so that comparisons take into account the important absolute measurements of the breath. An REML analysis was conducted to determine whether any differences existed between ‘‘normal’’ breaths and BRCs over time postexercise for normal horses. Period 1 was excluded because of a large breath-to-breath variation in tidal volumes. For most measurements, no significant difference was seen in BRCs. However, epz50%, epz75%, ipz75%, and Rf/(TE/TI) were different, suggesting that it is not appropriate to use ‘‘normal’’ breaths and BRCs after exercise in the same analyses. These results also confirm a functional difference between ‘‘normal’’ breaths and the BRCs described by Curtis et al17 with relative flow– time differences evident in late expiration and inspiration.
5. Dart AJ, Dowling BA, Hodgson DR, Rose RJ. Evaluation of highspeed treadmill videoendoscopy for diagnosis of upper respiratory tract dysfunction in horses. Aust Vet J 2001;79:109–112. 6. Kannegieter NJ, Dore ML. Endoscopy of the upper respiratory tract during treadmill exercise: a clinical study of 100 horses. Aust Vet J 1995;72:101–107. 7. Lumsden JM, Stick JA, Caron JJ, Nickels FA, Brown CM, Godber LM, et al. Upper airway function in performance horses: videoendoscopy during high-speed treadmill exercise. Comp Cont Educ Pract Vet 1995;17:1134–1143. 8. Wood JL, Newton JR, Chanter N, Mumford JA. Inflammatory airway disease, nasal discharge and respiratory infections in young British racehorses. Equine Vet J 2005;37:236–242. 9. Abramson AL, Goldstein MN, Stenzler A, Steele A. The use of the tidal breathing flow loop in laryngotracheal disease of neonates and infants. Latyngo 1982;92:922–926. 10. Connally BA, Derksen FJ. Tidal breathing flow-volume loop analysis as a test of pulmonary function in exercising horses. Am J Vet Res 1994;55:589–594. 11. Derksen FJ, Stick JA, Scott EA, Robinson NE, Slocombe RF. Effect of laryngeal hemiplegia and laryngoplasty on airway flow mechanics in exercising horses. Am J Vet Res 1986;47:16–20.
CONCLUSION In conclusion, comparisons between horses should not use breaths selected at random after exercise because of the effects of time postexercise and tidal volume, and the differences in BRCs. Only izp75% and Tpef/TE were fully independent. This study establishes guidelines for the selection of breaths after exercise and analysis of relative flow–time measurements in future studies of pulmonary function that investigate use of the indices. Further research is needed to determine whether the relationships between relative flow–time measurements and tidal volume, PIF, or PEF after exercise have relevance to routine pulmonary function testing in racehorses. ACKNOWLEDGMENTS The financial and personnel assistance by the Japan Racing Association is gratefully acknowledged. Technical developments that enabled conduct of the investigation were supported by the University of Sydney and Rural Industries Research and Development Corporation.
12. Guthrie AJ, Beadle RE, Bateman RD, White CE. The effects of three models of airway disease on tidal breathing flow-volume loops of Thoroughbred horses. Vet Res Commun 1995;19:517–527. 13. Ho¨rnicke H, Weber M, Schweiker W. Pulmonary ventilation in Thoroughbred horses at maximum performance. In: Gillespie JR, Robinson NE, eds. Equine exercise physiology 2. Davis, CA: ICEEP Publications; 1987:216–224. 14. Marlin DJ, Roberts CA. Qualitative and quantitative assessment of respiratory airflow and pattern of breathing in exercising horses. Equine Vet Educ 1998;10:178–186. 15. Pollmann U, Ho¨rnicke H. Characteristics of respiratory airflow during exercise in horses with reduced performance due to pulmonary emphysema or bronchitis. 760–771. 16. Evans DL, Marlin DJ. Pulmonary function testing. Equine Vet J 1999;30(Suppl):631–632. 17. Curtis RA, Kusano K, Evans DL, Lovell N. Observations on respiratory flow strategies during and after intense treadmill exercise to fatigue in thoroughbred racehorses. Equine Vet J 2006;36(Suppl):567–572. 18. Padilla DJ, McDonough P, Kindig CA, Erickson HH, Poole DC. Ventilatory dynamics and control of blood gases after maximal exercise in the Thoroughbred horse. J Appl Physiol 2004;96:2187–2193. 19. Curtis RA, Kusano K, Evans DL, Lovell NH, Hodgson DR. Reliabil-
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2005;169:223–231. 20. Landau L. Lung function testing in infancy. S Afr Respir J
inary study. Am J Vet Res 1981;42:703–707. 2. Raphel CF. Endoscopic findings in the upper respiratory tract of 479 horses. J Am Vet Med Assoc 1982;181:470–473.
1997;3:54–55. 21. Art T, Lekeux P. Training induced modifications in cardiorespiratory
3. Burrell MH, Mackintosh ME, Whitwell KE, Mumford JA, Rossdale
and ventilatory measurements in Thoroughbred horses. Equine Vet J
PD. A two year study of respiratory disease in a Newmarket stable: some preliminary observations. In: Proceedings Society for Veteri-
22. Butler PJ, Woakes AJ, Anderson LS, Roberts C, Marlin DJ. Stride
nary Epidemiology and Preventive Medicine; 1985:74–83. 4. Jeffcott LB, Rossdale PD, Freestone J, Frank CJ, Towers-Clark PF. An assessment of wastage in Thoroughbred racing from conception to 4 years of age. Equine Vet J 1982;14:185–198.
1993;25:532–536. length and respiratory tidal volume in exercising Thoroughbred horses. Resp Physiol 1993;93:51–56. 23. Couetil LL, Rosenthal FS, Simpson CM. Forced expiration: a test for airflow obstruction in horses. J Appl Physiol 2000;88:1870–1879.
ORIGINAL RESEARCH Relative Flow-Time Relationships in Single Breaths Recorded After Treadmill Exercise in Thoroughbred Horses K. Kusano, DVM,a R.A. Curtis, BSc SMIEEE,b C.A. Goldman, BScAgr,b and D.L. Evans, BVSc, PhDb ABSTRACT Analysis of individual breaths after exercise has potential for pulmonary function testing. The aims of this study were to investigate the dependence of measurements of pulmonary function in single breaths on time postexercise and tidal volume (VT) after treadmill exercise. Five Thoroughbred horses without evidence of airway disease were used. Horses had been previously acclimated to treadmill exercise and to wearing a face mask. A Quadflow spirometer recorded airflow rates continuously during 90 seconds after intense treadmill exercise to fatigue. Indices of function were based on ratios of times within each breath and analyses of the shape of relative flow–time curves within inspiration and expiration. Restricted maximum likelihood, general linear regression, repeated-measures one-way analysis of variance (ANOVA), and two sample t-tests were used, with statistical significance at P < .05. Time postexercise had no effect on several ratios based on time for inspiration (TI) and expiration (TE), and times to peak flows (TI/TT, TE/TT, TE/TI, Tpef [peak expiratory flow]/ TE, and Tpif [peak inspiratory flow]/TI). Many variables were significantly dependent on VT. Occasional big respiratory cycles with VT more than 10% greater than in the previous breath had significantly different means for relative flow (Rf)/(TE/TI), epz50% (50% of the time from Tpef to end of expiration), epz75% (75% of the time from Tpef to end of expiration), and ipz75% (75% of the time from Tpif to end of inspiration). Predicted means for these variables differed by 10–20%. This study establishes guidelines for the selection of breaths after exercise, and describes a new approach to measurement of relative flow and time relationships. It was concluded that several time-based ratios have potential for measuring pulmonary function. However,
From the Equine Department JRA, Tokyo, Japana; and the Faculty of Veterinary Science, The University of Sydney, New South Wales, Australia.b Reprint requests: R.A. Curtis, 4 Parkes St, Wentworth Falls, New South Wales, Australia. 0737-0806/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jevs.2007.06.005
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care is needed when selecting breaths for calculation of most of the new relative flow–time variables. Keywords: Respiratory; Physiology; Pulmonary; Breathing; Exercise
INTRODUCTION Respiratory tract disease is a common cause of poor performance in racing Thoroughbreds. Upper respiratory tract (URT) disorders have been identified as a contributor to suboptimal racing performance in 8.1%1 and 8.6%2 of horses. Inflammatory airway disease (IAD) is a more common cause of poor performance, interruption of training, and premature retirement in racehorses.3,4 In a population of young racehorses, the prevalence of IAD was 13.8% and the incidence was 8.9 cases/100 horses/month. Diagnosis of respiratory problems relies greatly on endoscopy at rest and during a high-speed treadmill examination5-7 and cytologic examinations.8 Diagnosis of respiratory limitation to performance does not usually include an assessment of limits to breathing, and therefore the degree of limitation to inspiration and expiration are not routinely quantified. In pulmonary function testing (PFT) of humans with suspected lower airway problems, the measurement of peak expiratory flow (PEF) rates and expired air volume in 1 second of a maximal, forced maneuver is commonly used. Maneuver techniques are, however, unsuitable for use in human infants and animals because cooperative compliance to the technique is not possible.9 Therefore, alternative methods also are required to quantify limits to breathing in racehorses. Findings in several studies encourage more research into development of indices of pulmonary function based on measurements in breath-by-breath spirometry during exercise.10-15 Development of techniques for assessment of pulmonary function based on measurements after exercise could increase the applicability of this approach in routine equine veterinary practice. Potentially, suitable measurements could diagnose limits to inspiration or expiration in different respiratory syndromes, assess the severity of a disease, and enable monitoring of responses to treatments. The PFT tests developed must be sensitive and accurate enough to detect subtle changes in respiratory Journal of Equine Veterinary Science Vol 27, No 8 (2007)
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function16 and to enable the differentiation of upper from lower airway breathing limitation. Curtis et al17 described different breath types during and after intense exercise on a treadmill. It was concluded that large breaths, or ‘‘big respiratory cycles’’ (BRCs), were a normal feature of pulmonary ventilation during and after intense exercise. These BRCs may not have the same relative time–flow shapes as the more usual, ‘‘normal’’ breaths, and care should be taken when selecting breaths recorded after exercise for analysis of pulmonary function. Padilla et al18 reported that postexercise hyperventilation in horses resulted in higher tidal volumes in the initial 13-second period of recovery. Tidal volumes within 30 seconds after exercise were similar to or greater than those recorded during prior intense treadmill exercise.17,18 Breaths after exercise may therefore be useful in pulmonary function tests because the lungs are functioning at tidal volumes similar to or greater than those found during intense exercise. Factors that influence the flow, time, and volume relationships in breaths after exercise should be studied to better understand their potential use in equine pulmonary function testing. Development of suitable indices of pulmonary function based on analyses of postexercise breaths could increase the applicability of this approach in veterinary practices. The following questions were addressed in this study: 1. How do measurements of pulmonary function in individual breaths depend on time after intense exercise? 2. Do measurements in BRCs after exercise differ from those in ‘‘normal’’ breaths? 3. Do measurements depend on tidal volume relative to body mass? This paper also describes a new approach to the evaluation of inspiration and expiration in a single breath, using relative flow–time relationships. This approach may obviate the need for production of maximal, forced inspirations or expirations to make a diagnosis if the shape of these relative flow–time relationships in single breaths after exercise depends on the health of the airways.
MATERIALS AND METHODS Five Thoroughbred horses were used in the study (2 male, 3 female; 3–8 years of age and mean body weight 483 kg 13 [SD]). All horses were acclimated to treadmill exercise, to wearing a face mask, and to exercise test protocols. The horses had been in regular treadmill training for 8 weeks before these tests of 5 days per week at speeds of 7–12 m/second. Horses were selected on the basis of tractability and absence of cardiac murmurs. They had no evidence of upper airway abnormalities during treadmill exercise at 12 m/second. No horses had lower airway disease based on tracheal wash results. Further details have been published.19 The experiments were approved by the Animal Use Committee of the Japan Racing Association. The Quadflow spirometer has been described previously.19 The flow sensors measured gas flow to 0.1 L/
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second resolution continuously every 10 milliseconds. Oxygen uptake was not calculated. The barometric pressure, ambient temperature, and relative humidity were recorded before each calibration of flows in left and right sensors. Airflow rates were recorded continuously during 90 seconds after intense treadmill exercise to fatigue. The exercise test consisted of stepped increases in treadmill speed until the horse was no longer able to maintain the same speed as the treadmill. Details of the treadmill exercise test protocol have been described.19 Measurements The Quadflow software measured inspiratory and expiratory flow (L/second) at 100 Hz, and a thermistor measured gas temperature at the nostrils. Barometric pressure, ambient temperature, and humidity were measured in the laboratory before each exercise test. The flow rates were corrected to body temperature and pressure, saturated with water vapor (BTPS). Tidal volume (VT), minute ventilation, and inspiratory and expiratory periods (TI, TE [seconds]) were calculated. Reliability of these measurements within and between horses using Quadflow hardware and software has been described.19 Three consecutive normal breaths were selected in each of the nine 10-second periods in the period immediately after exercise. A group of three breaths was selected from the last three breaths of each 10-second period, unless there was a BRC in that group. A BRC after exercise was defined as a breath having a tidal volume 10% greater than the previous breath.17 If a BRC occurred in the last 3 breaths of a time period, the previous three consecutive normal breaths within the period were selected for analysis. Means of several variables were calculated for each 10-second period (Table 1). The first of the three breaths was used to calculate the variables in Table 2. The parameter ezp25% refers to the percentage of the PEF at 25% of the time from commencement of expiration to the time at PEF (Tpef). Relative flows were also calculated for 50% and 75% of those relative times, and were expressed as ezp25%, ezp50%, and ezp75%. Similar relative flow-time measurements were made for 25%, 50%, and 75% of the time from Tpef to end of expiration (epz25%, epz50%, and epz75%). The same zp% and pz% measurements were made for the next inspiratory phase of the breath (izp25%, izp50%, izp75% and ipz25%, ipz50%, ipz75%). Each BRC in the second to the ninth 10-second interval was identified and the same variables were calculated for those breaths. Statistics Tidal volumes were expressed relative to body mass to help reduce that effect on the values. Restricted maximum likelihood (REML) analyses were used to determine whether significant differences existed between normal and large breaths. General linear regressions were conducted to determine whether measurements were dependent on tidal
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Table 1. Variables measured using mean values of 3 consecutive breaths in each 10-second period
Table 2. Relative flow-time variables calculated in one breath in each 10-second period
Name of Variable
Abbreviation
Description of Measurement
Abbreviations
Respiratory frequency Inspiratory period Expiratory period Time to peak inspiratory flow Time to peak expiratory flow Ratio of inspiratory time to total breath time Ratio of expiratory time to total breath time Ratio of time for expiration to time for inspiration Ratio of time to peak expiratory flow to expiratory time Ratio of time to peak inspiratory flow to inspiratory time Ratio of respiratory frequency to the ratio of TE/TI Peak inspiratory flow Peak expiratory flow Minute ventilation Tidal volume Inspired volume
Rf TI TE Tpif Tpef TI/TT
Percentage of PIF during the period of inspiration from zero flow to PIF Percentage of PIF at 25%, 50%, and 75% of the time taken to attain PIF Percentage of PIF during the period of inspiration from PIF to zero flow Percentage of decrease in PIF at 25%, 50%, and 75% of the time taken to decrease the PIF to zero flow rate Percentage of PEF during the period of expiration from zero flow to PEF Percentage of PEF at 25%, 50%, and 75% of the time taken to attain PEF Percentage of PEF during the period of expiration from PEF to zero flow Percentage of decrease in PEF at 25%, 50%, and 75% of the time taken to decrease the PEF to zero flow rate
izp
TE/TT TE/TI Tpef/Te Tpif/Ti Rf/(TE/TI) PIF PEF VE VT VTI
volumes. Repeated-measures one-way analyses of variance (ANOVA) were used to investigate whether there were significant effects of time postexercise. ANOVA and two-sample t-tests were performed using Sigma Stat 3.5, and all other analyses were performed using GenStat 8th edition. Statistical significance was set at P < .05.
RESULTS Tables 3 and 4 present the means ( SD) of the absolute and relative measurements in breaths studied in the nine 10-second time periods after exercise. Time postexercise had a significant effect on flow and tidal volume after exercise. Time periods 7, 8, and 9 were different (P < 0.05) from time period 1 for all variables. Variables TI, TE, and VTI were not different from each other for time periods 1 to 6. Time postexercise had no significant effect on TI/TT, TE/TT, TE/TI, Tpef/TE, and Tpif/TI. Figure 1 (A and B) shows typical relationships between relative times and percentages of PEF (ezp% and epz%) for expiration in a single breath recorded within 20 seconds after end of exercise. The PEF in this phase of the breath was 75 L/second, and TE was 468 milliseconds. Figure 2 (A and B) shows typical relationships between relative times and percentages of PIF (izp% and ipz%) for the next inspiration in the same breath described in Figure 1. The PIF in this phase was 52 L/second, and TI was 458 milliseconds. Table 5 presents the means (SD) of the epz% and ezp% relative flow rates at 25%, 50%, and 75% of the Tpef. No effects of time postexercise were seen on any variable in
izp25%, izp50%, izp75%
ipz
ipz25%, ipz50%, ipz75%
ezp
ezp25%, ezp50%, ezp75% epz
epz25%, epz50%, epz75%
Abbreviations: PEF, peak expiratory flow rate; PIF, peak inspiratory flow rate.
Table 5. Table 6 provides the means (SD) of the percentages of the izp% and ipz% relative flow rates at 25%, 50%, and 75% of the time taken to increase to peak flow, and the percentages of the decrease in peak flow at 25%, 50%, and 75% of the Tpif. Means for ipz50% in time periods 4, 5, and 7 were greater than in time period 1. Time postexercise had no effect on the other variables in Table 6. Many variables were dependent on tidal volume during recovery, including most of the pz% and zp% relative flow–time variables. BRCs had significantly different means for Rf/(TE/TI), epz50%, epz75%, and ipz75%. Predicted means for these variables in BRCs differed by 10–20% from normal breaths.
DISCUSSION This paper describes a new approach to evaluation of the inspiration and expiration in a single breath, using relative flow–time relationships, and reports on the influence of time postexercise and tidal volume after exercise on the measurements. An ideal measurement would be independent of time and tidal volume after exercise. Only two measurements, izp75% and Tpef/TE, met those criteria. These
Time Period 1
2
3
4
5
6
7
8
9
a
a
TI 0.459 0.092 0.439 0.089 0.426 0.099 0.417 0.099 0.379 0.084 0.360 0.071 0.342 0.076 0.334 0.067 0.336 0.038a TE 0.405 0.077 0.390 0.078 0.405 0.097 0.376 0.089 0.354 0.075 0.347 0.062 0.318 0.058a 0.316 0.059a,c 0.306 0.045 a,c a a,b a,b a,b a,b,c a,b,c,d a,b,c,d VT 25.2 4.05 22.1 4.35 18.9 3.14 17.5 3.10 16.0 2.82 15.5 2.04 13.6 2.03 13.3 2.21 12.4 1.77a,b,c,d VTI 21.8 2.82 19.3 2.63 16.5 1.64 15.3 2.15 13.5 2.15 12.7 1.83 11.2 1.27 a,b 11.1 1.17 a,b 10.9 1.18 a,b a a,b a,b a,b a,b a,b,c a,b PEF 80.8 6.95 74.3 4.77 66.3 6.39 64.8 6.26 64.1 6.07 62.7 5.84 60.1 6.89 61.5 5.02 59.7 4.32a,b,c PIF 68.1 4.47 60.7 6.21a,b 54.4 5.99a,b 50.4 6.54a,b 48.7 5.91a,b,c 48.5 6.77a,b,c 45.1 8.30a,b,c,d 46.2 5.46a,b,c 44.6 5.36a,b,c,d a a,b,c a,b,c a,b,c,d a,b,c,d Rf 72.0 15.26 75.5 16.84 76.0 17.88 79.7 19.36 85.6 20.03 87.5 17.04 93.9 18.75 95.1 18.13 95.3 11.78 a,b,c,d VE 1762.9 137.33 1594.6 134.30a 1370.9 179.33a,b 1356.8 147.95a,b 1310.4 160.00a,b 1322.8 165.98a,b 1261.6 192.29a,b 1242.1 159.88a,b 1176.2 141.11a,b,c,d Abbreviations: TI, inspiratory time (seconds); TE, expiratory time (seconds); VT, tidal volume (L, BTPS); VTI, inspired volume (L,BTPS); PEF, peak expiratory flow (L/second, BTPS); PIF, peak inspiratory flow (L/second, BTPS); Rf, respiratory frequency (breaths/minute); VE, minute ventilation (L/minute, BTPS). a Different from time period 1 (P < .05). b Different from time period 2 (P < .05). c Different from time period 3 (P < .05). d Different from time period 4 (P < .05).
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Table 3. Mean ( SD) of absolute measurements in breaths studies in nine 10-second time periods after exercise
Table 4. Mean ( SD) of relative measurements in nine 10-second time periods after exercise Time Period TI/TT TE/TT TE/TI Tpef/Te Tpif/Ti Rf/(TE/TI)
1
2
3
4
5
6
7
8
9
0.532 0.020 0.468 0.020 0.877 0.076 0.399 0.135 0.271 0.102 82.8 21.04
0.529 0.026 0.471 0.026 0.887 0.102 0.368 0.105 0.379 0.157 87.4 26.46
0.515 0.023 0.485 0.023 0.948 0.108 0.502 0.154 0.302 0.181 82.7 28.41
0.523 0.022 0.477 0.022 0.907 0.093 0.499 0.139 0.340 0.201 92.8 30.09
0.519 0.018 0.481 0.018 0.925 0.073 0.468 0.134 0.345 0.137 94.9 21.92
0.512 0.013 0.488 0.013 0.953 0.047 0.347 0.109 0.295 0.103 94.1 15.15
0.516 0.011 0.484 0.011 0.939 0.043 0.577 0.312 0.346 0.137 99.6 16.97a,c
0.513 0.009 0.487 0.009 0.950 0.035 0.452 0.150 0.396 0.184 100.1 18.35a,c
0.521 0.024 0.479 0.024 0.912 0.105 0.370 0.122 0.392 0.180 106.4 23.73a,b,c
Abbreviations: TI/TT, ratio of inspiratory time to breath duration; TE/TT, ratio of expiratory time to breath duration; TE/TI, ratio of time for expiration to time for inspiration; Tpef/Te, ratio of peak expiratory flow to expiratory time; Tpif/Ti, ratio of peak inspiratory flow to inspiratory time; Rf/(TE/TI), ratio of respiratory frequency to the ratio of TE/TI. a Different from time period 1 (P < .05). b Different from time period 2 (P < .05). c Different from time period 3 (P < .05).
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Figure 1. Relationship between relative time and percentage of peak flow rates for expiration (ezp%, epz%) in a single breath recorded within 20 seconds after end of exercise. A represents relative time and flows from zero flow to peak expiratory flow rate, and B represents relative time and flow rate from peak expiratory flow rate to zero flow rate.
Figure 2. Relationship between relative time and percentage of peak flow rates for inspiration (izp%, ipz%) in a single breath recorded within 20 seconds after end of exercise. A represents relative time and flows from zero flow to peak inspiratory flow rate, and B represents relative time and flow rate from peak inspiratory flow rate to zero flow rate.
results are a new contribution to knowledge concerning evaluation of pulmonary function in horses. The results provide guidance concerning selection of breaths after intense exercise for analysis of pulmonary function. They also provide guidelines for breath selection after exercise in future studies of relative flow–time relationships in studies that investigate the effects of various respiratory problems. Care is needed when selecting breaths after exercise because measurements were dependent on tidal volume and were different in BRCs. Pulmonary function tests based on analyses of postexercise breaths will need to consider both the absolute and relative measurements in conjunction, except for izp75% and Tpef/TE. The relevance of these two measurements to pulmonary function testing is not yet known, and further studies are required in more normal horses and horses with pulmonary dysfunction. Interestingly, the Tpef/TE ratio has recently been used to describe pulmonary function in human infants during normal quiet breathing.20 The basis for selecting breaths immediately after exercise was an expectation that tidal volumes would be greater than during exercise. As a consequence, the lungs would be functioning at closer to a vital capacity after exercise than during exercise. In the first 30 seconds after exercise, mean minute ventilation ranged from approximately
1,400–1,750 L/minute. Art and Lekeux21 reported minute ventilations in Thoroughbred horses during treadmill exercise at 9 m/second of 1,650–1,850 L/minute, with tidal volumes of 14–16 L. Butler et al22 reported similar values during treadmill exercise, and Ho¨rnicke et al13 reported tidal volumes of 10–13 L during maximal field exercise, with PEF and PIF of 67–76 and 56–68 L/second, respectively. Minute ventilations of over 2,000 L/minute were recorded during treadmill exercise at 10 m/second in a group of six horses.17 Those results included data obtained from five of the horses that were used in this study. Tidal volumes in the first 60 seconds after the completion of exercise in the current study were similar to or greater than previously reported values during exercise. These results confirm the potential for use of individual breaths during recovery after exercise for pulmonary function tests in horses. However, PEF and PIF were lower than measured during exercise in other studies. Couetil et al23 have estimated that vital capacities are greater than 40 L in large horses, and therefore it is unlikely that vital capacities would be approached, even during maximal ventilation in the 13-second period after intense exercise. A forced expiratory flow pulmonary function test has been used in resting horses to quantify limits to expiration in resting horses with IAD and chronic obstructive
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Table 5. Mean ( SD) percentages of peak flow rate at 25%, 50%, and 75% of time taken to increase flow to PEF (ezp25%, ezp50%, ezp75%), and percentages of the decrease in PEF at 25%, 50%, and 75% of time taken to decrease flow from PEF to zero flow rate (epz25%, epz50%, epz75%) % of PEF at 3 Relative Times to Attain PEF
% of PEF at 3 Relative Times to Decrease to 0 L/s
Time period
ezp25%
ezp50%
ezp75%
epz25%
epz50%
epz75%
1 2 3 4 5 6 7 8 9
0.56 0.141 0.54 0.175 0.66 0.210 0.60 0.222 0.55 0.123 0.44 0.143 0.58 0.183 0.52 0.083 0.41 0.122
0.86 0.090 0.84 0.111 0.89 0.110 0.87 0.114 0.85 0.068 0.79 0.111 0.87 0.096 0.85 0.070 0.74 0.146
0.96 0.029 0.95 0.046 0.96 0.017 0.95 0.026 0.94 0.024 0.95 0.016 0.95 0.014 0.96 0.019 0.92 0.094
0.92 0.030 0.94 0.024 0.91 0.061 0.93 0.051 0.92 0.017 0.88 0.053 0.90 0.108 0.92 0.036 0.89 0.069
0.77 0.120 0.86 0.089 0.74 0.081 0.80 0.088 0.74 0.056 0.73 0.097 0.75 0.068 0.74 0.121 0.70 0.165
0.62 0.235 0.61 0.169 0.49 0.155 0.49 0.120 0.46 0.152 0.54 0.144 0.49 0.070 0.46 0.185 0.47 0.140
pulmonary disease.23 The studies of expiratory flow curves in IAD cases had greater accuracy and sensitivity for diagnosis than tests using standard pulmonary mechanics. The challenge now is to ascertain whether accurate and sensitive measurements of pulmonary function can be made with analyses in breaths after exercise with tidal volumes that are likely to be less than 50% of vital capacity. To expect that measurements would be most useful in breaths in the first 13 seconds after intense exercise when tidal volumes will be greatest is logical.17,18 However, the mask would probably have to be worn by the horse during prior exercise to satisfactorily record those breaths. The findings by Couetil et al23 encourage further research into techniques for pulmonary function testing that evaluate respiratory air flow at submaximal tidal volumes. Time postexercise had no effect on many fractional time and relative flow–time variables (including TI/TT, TE/TT, TE/TI, Tpef/Te, Tpif/Ti, ezp25%, ezp50%, ezp75%, izp25%, izp50%, izp75%, epz25%, epz50%, epz75%, ipz25%, and ipz75%). For these variables, the Quadflow mask can be applied any time during the 90-second period after exercise. However, there was an effect of time postexercise for ipz50%. The importance of this measurement is yet to be
elucidated, but it could be an important index of limit to breathing during late inspiration. Application of the mask and recording breaths in the first 30 seconds would be desirable for measurements of ipz50%. To measure this variable, one must apply the mask as quickly as possible, or apply the mask before exercise. Significant differences were seen between all other variables over time postexercise. Therefore, comparisons between and within horses cannot be based on selection of breaths at random. A superior approach could be to express the relative time–flow measurements in relation to an absolute measurement in the same breath, such as tidal volume, PEF, or PIF. For example, future research could investigate whether the relationships between the relative flow–time measurements and the peak flow rate for the same breath are different in horses with respiratory problems. Such an approach has a precedent.15 Pulmonary function was described with individual breath analyses during lunging exercise in three groups of riding horses. Regressions of respiratory frequency on relative time ratios (TE/TI) were presented for normal horses and horses with bronchitis and pulmonary emphysema. This paper also referred to ‘‘position’’ of the PIF and PEF within the phase of the breath.
Table 6. Mean ( SD) percentages of peak flow rate at 25%, 50%, and 75% of time taken to increase flow to PIF (izp25%, izp50%, izp75%), and percentages of the decrease in PIF at 25%, 50%, and 75% of time taken to decrease flow from PIF to zero flow rate (ipz25%, ipz50%, ipz75%) % of PIF at 3 Relative Times to Attain PIF
% of PIF at 3 Relative Times to Decrease to 0 L/s
Time period
izp25%
izp50%
izp75%
ipz25%
ipz50%
ipz75%
1 2 3 4 5 6 7 8 9
0.46 0.088 0.57 0.065 0.42 0.097 0.48 0.139 0.51 0.163 0.41 0.111 0.45 0.169 0.47 0.078 0.49 0.098
0.80 0.050 0.93 0.106 0.76 0.076 0.80 0.085 0.82 0.106 0.76 0.086 0.79 0.112 0.79 0.050 0.80 0.059
0.96 0.014 0.97 0.012 0.95 0.024 0.95 0.026 0.96 0.022 0.94 0.034 0.96 0.023 0.93 0.034 0.95 0.033
0.86 0.064 0.91 0.054 0.90 0.076 0.94 0.058 0.92 0.040 0.88 0.086 0.92 0.051 0.92 0.090 0.93 0.052
0.73 0.069 0.79 0.062 0.81 0.068 0.86 0.062a 0.84 0.039a 0.82 0.064 0.84 0.038a 0.83 0.059 0.81 0.059
0.53 0.147 0.64 0.137 0.56 0.108 0.61 0.085 0.67 0.119 0.64 0.098 0.62 0.102 0.63 0.141 0.59 0.097
a
Different from time period 1 (P < .05).
K Kusano et al Vol 27, No 8 (2007)
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In our results, we present these ‘‘position’’ values as Tpef/ TE, and Tpif/TI. In Pollmann and Ho¨rnicke,15 the results suggested that Tpef/TE ratios might be lower in the more diseased horses. This finding could reflect a limit to flow in the early phase of expiration. Future studies could use the relative ezp% measurements to quantify relative flow in this phase of the breath with regressions on PEF or tidal volume, so that comparisons take into account the important absolute measurements of the breath. An REML analysis was conducted to determine whether any differences existed between ‘‘normal’’ breaths and BRCs over time postexercise for normal horses. Period 1 was excluded because of a large breath-to-breath variation in tidal volumes. For most measurements, no significant difference was seen in BRCs. However, epz50%, epz75%, ipz75%, and Rf/(TE/TI) were different, suggesting that it is not appropriate to use ‘‘normal’’ breaths and BRCs after exercise in the same analyses. These results also confirm a functional difference between ‘‘normal’’ breaths and the BRCs described by Curtis et al17 with relative flow– time differences evident in late expiration and inspiration.
5. Dart AJ, Dowling BA, Hodgson DR, Rose RJ. Evaluation of highspeed treadmill videoendoscopy for diagnosis of upper respiratory tract dysfunction in horses. Aust Vet J 2001;79:109–112. 6. Kannegieter NJ, Dore ML. Endoscopy of the upper respiratory tract during treadmill exercise: a clinical study of 100 horses. Aust Vet J 1995;72:101–107. 7. Lumsden JM, Stick JA, Caron JJ, Nickels FA, Brown CM, Godber LM, et al. Upper airway function in performance horses: videoendoscopy during high-speed treadmill exercise. Comp Cont Educ Pract Vet 1995;17:1134–1143. 8. Wood JL, Newton JR, Chanter N, Mumford JA. Inflammatory airway disease, nasal discharge and respiratory infections in young British racehorses. Equine Vet J 2005;37:236–242. 9. Abramson AL, Goldstein MN, Stenzler A, Steele A. The use of the tidal breathing flow loop in laryngotracheal disease of neonates and infants. Latyngo 1982;92:922–926. 10. Connally BA, Derksen FJ. Tidal breathing flow-volume loop analysis as a test of pulmonary function in exercising horses. Am J Vet Res 1994;55:589–594. 11. Derksen FJ, Stick JA, Scott EA, Robinson NE, Slocombe RF. Effect of laryngeal hemiplegia and laryngoplasty on airway flow mechanics in exercising horses. Am J Vet Res 1986;47:16–20.
CONCLUSION In conclusion, comparisons between horses should not use breaths selected at random after exercise because of the effects of time postexercise and tidal volume, and the differences in BRCs. Only izp75% and Tpef/TE were fully independent. This study establishes guidelines for the selection of breaths after exercise and analysis of relative flow–time measurements in future studies of pulmonary function that investigate use of the indices. Further research is needed to determine whether the relationships between relative flow–time measurements and tidal volume, PIF, or PEF after exercise have relevance to routine pulmonary function testing in racehorses. ACKNOWLEDGMENTS The financial and personnel assistance by the Japan Racing Association is gratefully acknowledged. Technical developments that enabled conduct of the investigation were supported by the University of Sydney and Rural Industries Research and Development Corporation.
12. Guthrie AJ, Beadle RE, Bateman RD, White CE. The effects of three models of airway disease on tidal breathing flow-volume loops of Thoroughbred horses. Vet Res Commun 1995;19:517–527. 13. Ho¨rnicke H, Weber M, Schweiker W. Pulmonary ventilation in Thoroughbred horses at maximum performance. In: Gillespie JR, Robinson NE, eds. Equine exercise physiology 2. Davis, CA: ICEEP Publications; 1987:216–224. 14. Marlin DJ, Roberts CA. Qualitative and quantitative assessment of respiratory airflow and pattern of breathing in exercising horses. Equine Vet Educ 1998;10:178–186. 15. Pollmann U, Ho¨rnicke H. Characteristics of respiratory airflow during exercise in horses with reduced performance due to pulmonary emphysema or bronchitis. 760–771. 16. Evans DL, Marlin DJ. Pulmonary function testing. Equine Vet J 1999;30(Suppl):631–632. 17. Curtis RA, Kusano K, Evans DL, Lovell N. Observations on respiratory flow strategies during and after intense treadmill exercise to fatigue in thoroughbred racehorses. Equine Vet J 2006;36(Suppl):567–572. 18. Padilla DJ, McDonough P, Kindig CA, Erickson HH, Poole DC. Ventilatory dynamics and control of blood gases after maximal exercise in the Thoroughbred horse. J Appl Physiol 2004;96:2187–2193. 19. Curtis RA, Kusano K, Evans DL, Lovell NH, Hodgson DR. Reliabil-
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