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Work of breathing in exercising ponies
Research in Veterinary Science 1989, 46, 49-53
Work of breathing in exercising ponies T. ART, P. LEKEUX, Laboratory jor Cardiopulmonary Functional Investigation, Faculty oj Veterinary Medicine, University of Liege, Brussels, Belgium
This paper attempts to evaluate the changes in the mechanical work of breathing induced by the increase of ventilation in ponies exercising on a treadmill. Airflow, tidal volume (VT) and oesophageal pressure were simultaneously recorded in eight ponies (four to six years old and weighing 258 ± 11 kg) before, during and after standardised exercise. Respiratory frequency, VT and minute volume (Ve) for each phase of the experimental protocol were calculated from the collected data. The pressure-volume diagrams were traced and the work per cycle (Wrm) was estimated by measuring the area enclosed in the loop. The work per minute (Wrm) and the work per litre of ventilation (Wrm litre l) were also calculated. From rest to fast trot Wrm litre -I, Wrm and Wrm had increased 8· 1, 13· 0 and 55' 6 times, respectively. The relationships between Ve and Wrm litre " ! was linear and that between Ve and Wrm curvilinear. Results suggested that the mechanical cost of the work of breathing could be a limiting or at least a constraining factor of the increase of ventilation during strenuous exercise in ponies. r
THE increase of ventilation during exercise requires increased activity of the respiratory muscles. The mechanical cost of providing these ventilatory requirements could be a source of constraint and potential limitation of ventilation (Whipp and Pardy 1986). Otis (1954), Margaria et al (1960) and Shephard (1966) have pointed out that during strenuous exercise, any further increase of ventilation above a certain critical level will not render more energy available for work other than the work of breathing. The classical approach to the assessment of respiratory muscle activity is based on the simultaneous recording of pulmonary volume and intrathoracic pressure variations (Rohrer 1916, Rahn et al 1946, Campbell 1958). Although it is known that the total work of breathing (especially during ventilation at a high level) is underestimated by this method, the latter gives a good estimation of the dynamic components of the work of breathing (Margaria et al 1960). Therefore, this method was used to estimate the work of breathing in resting horses (Willoughby and McDonell 1979) as well as in exercising athletes 49
(Margaria et al 1960, Milic-Emili et al 1962). Such investigations have never been reported as regards exercising horses. The purpose of this experiment was to investigate the effects of increasing ventilation on the work of breathing in eight ponies performing a treadmill exercise of graded intensity. Materials and methods Eight ponies, from four to six years old and weighing 258 ± II kg, were used. They were considered as healthy on the basis of clinical, endoscopical and arterial blood gas examinations. One month before the experiment, they were dewormed and vaccinated against tetanus and influenza. The pulmonary function tests were performed according to the technique, standardisation and calibrations previously reported (Art and Lekeux 1988)and briefly described. Respiratory airflow (V) and tidal volume (VT) were measured with Fleisch pneumotachographs number 4 (at rest) and number 5 (during exercise) fixed on a face mask and connected to a differential pressure transducer (Gould) with two identical polyethylene catheters. This assembly allowed the continuous recording of V, which was electronically integrated with respect to time to give VT. Pleural pressure was. recorded by means of an oesophageal balloon catheter put into the middle thoracic oesophagus and connected to a pressure transducer (Gould). Respiratory airflow, VT and oesophageal pressure changes (Pes) were simultaneously recorded on a rapid writing polygraph (Gould ES 1000). All the transducers were carefully calibrated (both statically and dynamically) and checked for phase compatibility before and after each experimental protocol. Experiments were performed on a treadmill (incline 8· 3 0) located outdoors. The experimental protocol was standardised and consisted of a five minute rest period, a two minute walk (I. 5 m S-I), a three minute slow trot (3' 0 m s- I), a three minute fast trot (3' 5 m S-I) and five minute recovery. All parameters were recorded at rest, at the end of each work period, after stopping and after five minutes recovery. Calculations were derived from measurements of five regular respiratory cycles. Respiratory frequency
T. Art, P. Lekeux
50
TABLE 1: Mechanical work of breathing (Wrm) calculated on the basis of Pes and Ppl Value Wrm IPesl
Unit
J
x SEM
WrmlPpl)
J
x SEM
Rest
Walk
Trot 1
Trot 2
1·15 0·16
4·84 0·30
10·60 0·34
12·65 1·81
1·07 0·19
4·17 0·35
10·48 0·38
12·46 1·52
(0, VT and minute volume eVe) were measured for each period. On the other hand, pressure-volume diagrams were traced from the Pes and the VT curves. The mechanical work of breathing (Wm) was estimated by measuring the area enclosed by the pressure-volume loops (Campbell 1958). The work per minute (Wrrn) and the work per litre of ventilation (Wrrn litre-I) were also calculated. In order to assess the validity of the calculation of Wrm on the basis of Pes, the intrapleural pressure (Ppl) was measured directly by pleural puncturing in four of the eight ponies. The Wrm was estimated on the basis of the Pes and the Ppl curves for each gait, and values were compared using a one-way analysis of variance.
60
50
•
E8
Wrm litre- 1
Wrm [ ] Wrm
40
#. 30
20
10
Rest
Walk
Trot 1
Trot 2
Stop
5 min
FIG 1: Relative values of work per litre of ventilation (Wrm litre l) work per cycle IWrm) and minute work (Wrml at rest, during exercise and recovery. Data are related to resting values r
Results
The work calculated on the basis of Pes was not significantly different from that calculated on the basis of Ppl (Table I). Respiratory frequency, VT, Ve and Wrm at rest, during and after exercise are given in Table 2. Wrm Iitre:", Wrm and Wrrn at a fast trot were, respectively, 8· I, 13· 0 and 55' 6 times greater than at rest (Fig I). There was a curvilinear relation between Wrm and Ve (Fig 2) and a linear relation between Wrm litre- I and Ve (Fig 3). The pressure-volume loops of one pony at rest and during each phase of the exercise are shown in Fig 4. Discussion
The validity of the method used 'for the measure-
ment of Pes, Ppl, V and VT, as well as the accuracy of the measurement of the intrathoracic pressure changes by means of an oesophageal balloon, were demonstrated in a previous paper (Art and Lekeux 1988). The present experiment assesses the accuracy of the estimation of Wrm on the basis of Pes changes. There is no method for directly measuring the total mechanical work performed during spontaneous breathing (Roussos and Campbell 1986). The catheter balloon technique is the most common method of measuring simultaneous changes in VT and Ppl (Milic-Emili et aI1964). Thus work is calculated from the area enclosed by the pressure-volume loop (Campbell 1958). However, this technique is only reliable when all elastic potential energy stored during
TABLE 2: Respiratory frequency (f). tidal volume (VTl. minute volume rite) and mechanical work per cycle (Wrm) in eight ponies at rest. during and after exercise Value
Unit min- 1
x SEM
VT
Litre
x SEM
Ve
Litre min- 1
x SEM
Wrm
J
x SEM
Rest
Walk
Trot 1
Trot 2
Stop
5 minutes
27·37 5·75
71·5 7·15
95·2 10·6
110·12 8·6
69·4 8·1
66·0 11·6
2·8 0·25
3·5 0·19
7004 10·7 1·08 0·18
247·1 24·7
4042 0·26
4·5 0·14 427·8 35·0 10·77 1·00
4·3 0·21 473·2 23·8 14·14 1·5
4·6 0·32 312·9 30·2
704 1·7
2·3 0·25 138·6 18·5 1·19 0·21
Work of breathing in exercising ponies 2000
El
A
• B • C • D •o E F .... G
'" H
~ 'E ::! 1000 E
.~
o-F;..,'T--.-------,----,.--,----.-..., 600 o 200 400 Ve (litre rnirr")
FIG 2: Individual curves of the relationship between the minute work (Wrm) and the minute volume I'Ve) in eight ponies, Ponies are designated by letters A to H
51
increases the elastic work of breathing (Milic-Emili et al 1960), while the second increases the flow-resistive work of breathing. In human medicine the existence of an optimal rate of f at which alveolar ventilation can be maintained with a minimal expenditure of respiratory work was demonstrated theoretically and experimentally (Rohrer 1916, Otis 1954, Mead 1960). Unfortunately, this fact is difficult to prove in horses because of their lack of cooperation. However, when accelerating from trot I to trot 2, the ponies further increased their ventilation by increasing f and slightly decreasing VT. This suggests that in this species as well as in humans, the interrelation of f and VT could be regulated so that the work of breathing would tend to be minimised or optimised . The minute mechanical work of breathing for high levels of ventilation, where expiration is active, increases with the cube of v« (Otis et al 1950), the latter representing the work done in overcoming the resistance to turbulent V. A recent study of Attenburrow et al (1983) established that in an equine trachea, the critical V, above which turbulent V can be anticipated, equals l' 3 litre s- I. Thus during exercise, V in the trachea will be turbulent throughout almost the entire respiratory cycle. Another factor which could be responsible for the increase of Wrm is the increase of the inertial forces 4
y
=
0·174 + O'OO6x R2
=
0·99
inspiration is used in overcoming dynamic resistance m during expiration (Margaria et al 1960). On the other 3 hand, it underestimates the total work of breathing, on account of the following facts. It is not possible to measure flow-resistive work done to the thorax, which according to some authors can account for 28 to 36 per cent of the total mechanical work (Opie et al ~ 1959, Bergofsky 1964). Similarly, it is not possible to ::! 2 estimate the elastic work done to the chest wall. ~ Moreover, the displacement of the abdominal E contents may be quite large and forces due to the ~ consequent distortions are not measured (Goldman et a al 1976). Lastly, because changes in volume are measured at the mouth, the work done in compressing and decompressing gas in the lungs is not included (Otis 1954, Jaeger and Otis 1964). The manner in which the work of breathing increases with exercise' depends upon two main factors: (a) the relative El change in the rate and depth of respiration as Ve increases and (b) the effect of exercise on the O;--<-r--,---.--r----.---,-r---,---.----, magnitude of the resistance (McIlroy et al 1954). o 100 200 300 400 500 When the ponies were exercising at low intensity, Ve (litre min") the increase of Ve was due to the simultaneous FIG 3: Relationship between the work per litre ventilation (Wrm increase of VT and f (Table 2). The first factor litre -1) and the minute volume (Ve)
52
T. Art, P. Lekeux 2
2
iii
iii
='"'"
a..
='"
a..
0
'"
a..
0
a..
-1
-2
2
-1
2 3 4 Vr (litre)
0
-2 5
='"
2 3 4 Vr (litre)
0
C
2
5
D
iii
iii
='"'"
a..
a..
'"
B
A
0
0
a..
a..
-1
-1
2345
vv (litre)
2345
vv (litre)
FIG 4: Pressure-volume loops from one pony at rest (AI and during exercise (B walk, C trot 1, D trot 21. I Inspiration, E Expiration
resulting from the increase of the V acceleration. Studies performed on humans suggested that in this species, the inertial forces may be considered as negligible factors in the increase of Wrrn, even during high levels of ventilation (Dubois et al 1956, Dosman et al 1975). However, this could be false as regards large animals during fast breathing (Lekeux et al 1988). The negative slope of the compliance line supports this assumption (Mead 1956) and may not be attributed to a technical inaccuracy since all the pressure transducer-catheters systems were phasetested before and after each experiment (Art and Lekeux 1988). Other factors such as distortional forces, flowresistive and elastic forces on the thorax, and displacement of the abdominal content (Goldman et al 1976) also contribute to the increase of the total work of breathing; unfortunately they are difficult to investigate in uncooperative subjects such as horses. In humans, at levels of ventilation commonly achieved during exercise, the total work of breathing may be underestimated by up to 25 per cent in the Campbell diagram (Goldman et al 1976). It is likely
that this phenomenon is the same in horses because of the stiffness of their chest wall (Leith and Gillespie 1971). However, the study of the volume displacement of the rib cage and abdomen during exercise as well as the determination of the static pressure of the chest wall would be necessary to confirm this assumption. In the present ponies as well as in athletes, the relationship between the mechanical work of breathing per unit volume of ventilation and the minute volume is approximated by a straight line (Goldman et al 1976). On the other hand, the relationship between Wrrn and Ve was curvilinear with an upward concavity (Fig 2). These curves were of ever-increasing slope. This implies that the mechanical cost of breathing for any additional units of air ventilated becomes greater with any increase of ventilation. This observation is also in good agreement with previous studies performed on human beings (Margaria et al 1960, Milic-Emili et al 1962, Goldman et al 1976). Previous studies performed on highly trained subjects suggest that at a high level of ventilation there is a threshold which represents the maximum value available for useful external work: any further increase of ventilation will not make more oxygen available without lowering the arterial oxygen pressure (Pa02) (Margaria et al 1960, Shephard 1966). The four facts that the rate of Wrrn increased in a curvilinear way with increasing ventilation, by the method used in this study, the total work of breathing is underestimated, the exertion of the present ponies was submaximal, and workers recently reported a decrease in Pao2 in horses during maximal exercise (Bayly et al 1983, Manohar 1986) suggest that during maximal exercise the work of breathing in this species could also be a limiting or, at least, a constraining factor on increasing ventilation. Nevertheless, this assumption has to be confirmed by the simultaneous study of the exercise-induced changes in the mechanical work and oxygen cost of breathing. .. Acknowledgements The authors thank the PMU Beige for its financial support and M. Leblond for her technical assistance. References ART, T. & LEKEUX, P. (1988) Veterinary Research Communication 12,25-39 ATTENBURROW, D. P., FLACK, F. c.. HbRNICKE, H., MEIXNER, R. & POLLMAN, U. (1983) Equine Exercise Physiology. Eds D. H. Snow, S. G. B. Personn & R. J. Rose. Cambridge, Granta Editions. pp 23-26 BAYLY, W. M., GRANT, B. D., BREEZE, R. G. & KRAMER, J. w. (1983) Equine Exercise Physiology. Eds D. H. Snow, S. G. B. Persson & R. J. Rose. Cambridge, Granta Editions. pp 400-407
Work of breathing in exercising ponies BERGOFSKY, E. H. (1964) Journal of Applied Physiology 19, 698-706 CAMPBELL, E. J. M. (1958) The Respiratory Muscles and the Mechanics of Breathing. Chicago. Year Book DUBOIS, A. B., BRODY, A. W., LEWIS, D. H. & BURGESS, B. F. (1956) Journal of Applied Physiology 8, 587-594 DOSMAN, J., BODE, F., URBANETTI, J., ANTIC, R., MARTIN, R. & MACKLEM, P. T. (1975) Journal of Applied Physiology 38, 64-69 GOLDMAN, M. D., GRIMBY, G. & MEAD, J. (1976) Journal of Applied Physiology 41,752-763 JAEGER, M. J. & OTIS, A. B. (1964) Journal of Applied Physiology 19, 83-91 LEITH, D. E. & GILLESPIE, J. R. (1971) Federation Proceedings 30,551 LEKEUX, P., ART, T., CLERCX, C, GUSTIN, P. (1988) Veterinary Research Communications 12, 61-66 McILROY, M. B., MARSHALL, R. & CHRISTIE, R. V. (1954) Clinical Sciences 13, 127-136 MANOHAR, M. (1986) American Journal of Veterinary Research 47,1387-1394 MARGARIA, R., MILlC-EMILI, G., PETIT, J. M. & CAVAGNA, G. (1960) Journal of Applied Physiology 15, 354-358 MEAD, J. (1956) Journal of Applied Physiology 9, 208-212 MEAD, J. (1960) Journal of Applied Physiology 15, 325-336 MILlC-EMILI, G., MEAD, J. & TURNER, J. M. (1964) Journal of Applied Physiology 19, 212-216
53
MILlC-EMILI, G., PETIT, J. M. & DEROANNE, R. (1960) Internationales Zentralblutt fur Angnewandte Physiologie und Eindschluss Arbeitsphysiologie 18, 330- 340 MILlC-EMILI, G., PETIT, J. M. & DEROANNE, R. (1962) Journal of Applied Physiology 17,43-46 OPIE, L. H., SPLADlNG, J. M. K. & SCOTT, F. D. (1959) Lancet r, 545-550 OTIS, A. B. (1954) Physiology Review 34, 449-458 OTIS, A. B., FENN, W. O. & RAHN, H. (1950) Journal of Applied Physiology 2, 592-607 RAHN, H., OTIS, A. B., CHADWICK, L. E. & FENN, W. O. (1946) American Journal of Physiology 146, 161-178 ROHRER, F. (1916) Pflugers Archiv 165, 419 ROUSSOS, C & CAMPBELL, E. J. (1986) Handbook of Physiology - The Respiratory System llI, Mechanics of Breathing, pan 2. Baltimore, American Physiology Society. pp 481-509 SHEPHARD, R. J. (1966) Quarterly Journal of Experimental Physiology 51, 336-350 WHIPP, B. J. & PARDY, R. L. (1986) Handbook of PhysiologyThe Respiratory System Ill, Mechanics of Breathing, part 2. Baltimore, American Physiology Society. p 605 WILLOUGHBY, R. A. & McDONELL, W. N. (1979) Veterinary Clinics of North America: Large Animal Practice I, 171-196
Received October /4, 1987 Accepted February 7, 1988
Work of breathing in exercising ponies T. ART, P. LEKEUX, Laboratory jor Cardiopulmonary Functional Investigation, Faculty oj Veterinary Medicine, University of Liege, Brussels, Belgium
This paper attempts to evaluate the changes in the mechanical work of breathing induced by the increase of ventilation in ponies exercising on a treadmill. Airflow, tidal volume (VT) and oesophageal pressure were simultaneously recorded in eight ponies (four to six years old and weighing 258 ± 11 kg) before, during and after standardised exercise. Respiratory frequency, VT and minute volume (Ve) for each phase of the experimental protocol were calculated from the collected data. The pressure-volume diagrams were traced and the work per cycle (Wrm) was estimated by measuring the area enclosed in the loop. The work per minute (Wrm) and the work per litre of ventilation (Wrm litre l) were also calculated. From rest to fast trot Wrm litre -I, Wrm and Wrm had increased 8· 1, 13· 0 and 55' 6 times, respectively. The relationships between Ve and Wrm litre " ! was linear and that between Ve and Wrm curvilinear. Results suggested that the mechanical cost of the work of breathing could be a limiting or at least a constraining factor of the increase of ventilation during strenuous exercise in ponies. r
THE increase of ventilation during exercise requires increased activity of the respiratory muscles. The mechanical cost of providing these ventilatory requirements could be a source of constraint and potential limitation of ventilation (Whipp and Pardy 1986). Otis (1954), Margaria et al (1960) and Shephard (1966) have pointed out that during strenuous exercise, any further increase of ventilation above a certain critical level will not render more energy available for work other than the work of breathing. The classical approach to the assessment of respiratory muscle activity is based on the simultaneous recording of pulmonary volume and intrathoracic pressure variations (Rohrer 1916, Rahn et al 1946, Campbell 1958). Although it is known that the total work of breathing (especially during ventilation at a high level) is underestimated by this method, the latter gives a good estimation of the dynamic components of the work of breathing (Margaria et al 1960). Therefore, this method was used to estimate the work of breathing in resting horses (Willoughby and McDonell 1979) as well as in exercising athletes 49
(Margaria et al 1960, Milic-Emili et al 1962). Such investigations have never been reported as regards exercising horses. The purpose of this experiment was to investigate the effects of increasing ventilation on the work of breathing in eight ponies performing a treadmill exercise of graded intensity. Materials and methods Eight ponies, from four to six years old and weighing 258 ± II kg, were used. They were considered as healthy on the basis of clinical, endoscopical and arterial blood gas examinations. One month before the experiment, they were dewormed and vaccinated against tetanus and influenza. The pulmonary function tests were performed according to the technique, standardisation and calibrations previously reported (Art and Lekeux 1988)and briefly described. Respiratory airflow (V) and tidal volume (VT) were measured with Fleisch pneumotachographs number 4 (at rest) and number 5 (during exercise) fixed on a face mask and connected to a differential pressure transducer (Gould) with two identical polyethylene catheters. This assembly allowed the continuous recording of V, which was electronically integrated with respect to time to give VT. Pleural pressure was. recorded by means of an oesophageal balloon catheter put into the middle thoracic oesophagus and connected to a pressure transducer (Gould). Respiratory airflow, VT and oesophageal pressure changes (Pes) were simultaneously recorded on a rapid writing polygraph (Gould ES 1000). All the transducers were carefully calibrated (both statically and dynamically) and checked for phase compatibility before and after each experimental protocol. Experiments were performed on a treadmill (incline 8· 3 0) located outdoors. The experimental protocol was standardised and consisted of a five minute rest period, a two minute walk (I. 5 m S-I), a three minute slow trot (3' 0 m s- I), a three minute fast trot (3' 5 m S-I) and five minute recovery. All parameters were recorded at rest, at the end of each work period, after stopping and after five minutes recovery. Calculations were derived from measurements of five regular respiratory cycles. Respiratory frequency
T. Art, P. Lekeux
50
TABLE 1: Mechanical work of breathing (Wrm) calculated on the basis of Pes and Ppl Value Wrm IPesl
Unit
J
x SEM
WrmlPpl)
J
x SEM
Rest
Walk
Trot 1
Trot 2
1·15 0·16
4·84 0·30
10·60 0·34
12·65 1·81
1·07 0·19
4·17 0·35
10·48 0·38
12·46 1·52
(0, VT and minute volume eVe) were measured for each period. On the other hand, pressure-volume diagrams were traced from the Pes and the VT curves. The mechanical work of breathing (Wm) was estimated by measuring the area enclosed by the pressure-volume loops (Campbell 1958). The work per minute (Wrrn) and the work per litre of ventilation (Wrrn litre-I) were also calculated. In order to assess the validity of the calculation of Wrm on the basis of Pes, the intrapleural pressure (Ppl) was measured directly by pleural puncturing in four of the eight ponies. The Wrm was estimated on the basis of the Pes and the Ppl curves for each gait, and values were compared using a one-way analysis of variance.
60
50
•
E8
Wrm litre- 1
Wrm [ ] Wrm
40
#. 30
20
10
Rest
Walk
Trot 1
Trot 2
Stop
5 min
FIG 1: Relative values of work per litre of ventilation (Wrm litre l) work per cycle IWrm) and minute work (Wrml at rest, during exercise and recovery. Data are related to resting values r
Results
The work calculated on the basis of Pes was not significantly different from that calculated on the basis of Ppl (Table I). Respiratory frequency, VT, Ve and Wrm at rest, during and after exercise are given in Table 2. Wrm Iitre:", Wrm and Wrrn at a fast trot were, respectively, 8· I, 13· 0 and 55' 6 times greater than at rest (Fig I). There was a curvilinear relation between Wrm and Ve (Fig 2) and a linear relation between Wrm litre- I and Ve (Fig 3). The pressure-volume loops of one pony at rest and during each phase of the exercise are shown in Fig 4. Discussion
The validity of the method used 'for the measure-
ment of Pes, Ppl, V and VT, as well as the accuracy of the measurement of the intrathoracic pressure changes by means of an oesophageal balloon, were demonstrated in a previous paper (Art and Lekeux 1988). The present experiment assesses the accuracy of the estimation of Wrm on the basis of Pes changes. There is no method for directly measuring the total mechanical work performed during spontaneous breathing (Roussos and Campbell 1986). The catheter balloon technique is the most common method of measuring simultaneous changes in VT and Ppl (Milic-Emili et aI1964). Thus work is calculated from the area enclosed by the pressure-volume loop (Campbell 1958). However, this technique is only reliable when all elastic potential energy stored during
TABLE 2: Respiratory frequency (f). tidal volume (VTl. minute volume rite) and mechanical work per cycle (Wrm) in eight ponies at rest. during and after exercise Value
Unit min- 1
x SEM
VT
Litre
x SEM
Ve
Litre min- 1
x SEM
Wrm
J
x SEM
Rest
Walk
Trot 1
Trot 2
Stop
5 minutes
27·37 5·75
71·5 7·15
95·2 10·6
110·12 8·6
69·4 8·1
66·0 11·6
2·8 0·25
3·5 0·19
7004 10·7 1·08 0·18
247·1 24·7
4042 0·26
4·5 0·14 427·8 35·0 10·77 1·00
4·3 0·21 473·2 23·8 14·14 1·5
4·6 0·32 312·9 30·2
704 1·7
2·3 0·25 138·6 18·5 1·19 0·21
Work of breathing in exercising ponies 2000
El
A
• B • C • D •o E F .... G
'" H
~ 'E ::! 1000 E
.~
o-F;..,'T--.-------,----,.--,----.-..., 600 o 200 400 Ve (litre rnirr")
FIG 2: Individual curves of the relationship between the minute work (Wrm) and the minute volume I'Ve) in eight ponies, Ponies are designated by letters A to H
51
increases the elastic work of breathing (Milic-Emili et al 1960), while the second increases the flow-resistive work of breathing. In human medicine the existence of an optimal rate of f at which alveolar ventilation can be maintained with a minimal expenditure of respiratory work was demonstrated theoretically and experimentally (Rohrer 1916, Otis 1954, Mead 1960). Unfortunately, this fact is difficult to prove in horses because of their lack of cooperation. However, when accelerating from trot I to trot 2, the ponies further increased their ventilation by increasing f and slightly decreasing VT. This suggests that in this species as well as in humans, the interrelation of f and VT could be regulated so that the work of breathing would tend to be minimised or optimised . The minute mechanical work of breathing for high levels of ventilation, where expiration is active, increases with the cube of v« (Otis et al 1950), the latter representing the work done in overcoming the resistance to turbulent V. A recent study of Attenburrow et al (1983) established that in an equine trachea, the critical V, above which turbulent V can be anticipated, equals l' 3 litre s- I. Thus during exercise, V in the trachea will be turbulent throughout almost the entire respiratory cycle. Another factor which could be responsible for the increase of Wrm is the increase of the inertial forces 4
y
=
0·174 + O'OO6x R2
=
0·99
inspiration is used in overcoming dynamic resistance m during expiration (Margaria et al 1960). On the other 3 hand, it underestimates the total work of breathing, on account of the following facts. It is not possible to measure flow-resistive work done to the thorax, which according to some authors can account for 28 to 36 per cent of the total mechanical work (Opie et al ~ 1959, Bergofsky 1964). Similarly, it is not possible to ::! 2 estimate the elastic work done to the chest wall. ~ Moreover, the displacement of the abdominal E contents may be quite large and forces due to the ~ consequent distortions are not measured (Goldman et a al 1976). Lastly, because changes in volume are measured at the mouth, the work done in compressing and decompressing gas in the lungs is not included (Otis 1954, Jaeger and Otis 1964). The manner in which the work of breathing increases with exercise' depends upon two main factors: (a) the relative El change in the rate and depth of respiration as Ve increases and (b) the effect of exercise on the O;--<-r--,---.--r----.---,-r---,---.----, magnitude of the resistance (McIlroy et al 1954). o 100 200 300 400 500 When the ponies were exercising at low intensity, Ve (litre min") the increase of Ve was due to the simultaneous FIG 3: Relationship between the work per litre ventilation (Wrm increase of VT and f (Table 2). The first factor litre -1) and the minute volume (Ve)
52
T. Art, P. Lekeux 2
2
iii
iii
='"'"
a..
='"
a..
0
'"
a..
0
a..
-1
-2
2
-1
2 3 4 Vr (litre)
0
-2 5
='"
2 3 4 Vr (litre)
0
C
2
5
D
iii
iii
='"'"
a..
a..
'"
B
A
0
0
a..
a..
-1
-1
2345
vv (litre)
2345
vv (litre)
FIG 4: Pressure-volume loops from one pony at rest (AI and during exercise (B walk, C trot 1, D trot 21. I Inspiration, E Expiration
resulting from the increase of the V acceleration. Studies performed on humans suggested that in this species, the inertial forces may be considered as negligible factors in the increase of Wrrn, even during high levels of ventilation (Dubois et al 1956, Dosman et al 1975). However, this could be false as regards large animals during fast breathing (Lekeux et al 1988). The negative slope of the compliance line supports this assumption (Mead 1956) and may not be attributed to a technical inaccuracy since all the pressure transducer-catheters systems were phasetested before and after each experiment (Art and Lekeux 1988). Other factors such as distortional forces, flowresistive and elastic forces on the thorax, and displacement of the abdominal content (Goldman et al 1976) also contribute to the increase of the total work of breathing; unfortunately they are difficult to investigate in uncooperative subjects such as horses. In humans, at levels of ventilation commonly achieved during exercise, the total work of breathing may be underestimated by up to 25 per cent in the Campbell diagram (Goldman et al 1976). It is likely
that this phenomenon is the same in horses because of the stiffness of their chest wall (Leith and Gillespie 1971). However, the study of the volume displacement of the rib cage and abdomen during exercise as well as the determination of the static pressure of the chest wall would be necessary to confirm this assumption. In the present ponies as well as in athletes, the relationship between the mechanical work of breathing per unit volume of ventilation and the minute volume is approximated by a straight line (Goldman et al 1976). On the other hand, the relationship between Wrrn and Ve was curvilinear with an upward concavity (Fig 2). These curves were of ever-increasing slope. This implies that the mechanical cost of breathing for any additional units of air ventilated becomes greater with any increase of ventilation. This observation is also in good agreement with previous studies performed on human beings (Margaria et al 1960, Milic-Emili et al 1962, Goldman et al 1976). Previous studies performed on highly trained subjects suggest that at a high level of ventilation there is a threshold which represents the maximum value available for useful external work: any further increase of ventilation will not make more oxygen available without lowering the arterial oxygen pressure (Pa02) (Margaria et al 1960, Shephard 1966). The four facts that the rate of Wrrn increased in a curvilinear way with increasing ventilation, by the method used in this study, the total work of breathing is underestimated, the exertion of the present ponies was submaximal, and workers recently reported a decrease in Pao2 in horses during maximal exercise (Bayly et al 1983, Manohar 1986) suggest that during maximal exercise the work of breathing in this species could also be a limiting or, at least, a constraining factor on increasing ventilation. Nevertheless, this assumption has to be confirmed by the simultaneous study of the exercise-induced changes in the mechanical work and oxygen cost of breathing. .. Acknowledgements The authors thank the PMU Beige for its financial support and M. Leblond for her technical assistance. References ART, T. & LEKEUX, P. (1988) Veterinary Research Communication 12,25-39 ATTENBURROW, D. P., FLACK, F. c.. HbRNICKE, H., MEIXNER, R. & POLLMAN, U. (1983) Equine Exercise Physiology. Eds D. H. Snow, S. G. B. Personn & R. J. Rose. Cambridge, Granta Editions. pp 23-26 BAYLY, W. M., GRANT, B. D., BREEZE, R. G. & KRAMER, J. w. (1983) Equine Exercise Physiology. Eds D. H. Snow, S. G. B. Persson & R. J. Rose. Cambridge, Granta Editions. pp 400-407
Work of breathing in exercising ponies BERGOFSKY, E. H. (1964) Journal of Applied Physiology 19, 698-706 CAMPBELL, E. J. M. (1958) The Respiratory Muscles and the Mechanics of Breathing. Chicago. Year Book DUBOIS, A. B., BRODY, A. W., LEWIS, D. H. & BURGESS, B. F. (1956) Journal of Applied Physiology 8, 587-594 DOSMAN, J., BODE, F., URBANETTI, J., ANTIC, R., MARTIN, R. & MACKLEM, P. T. (1975) Journal of Applied Physiology 38, 64-69 GOLDMAN, M. D., GRIMBY, G. & MEAD, J. (1976) Journal of Applied Physiology 41,752-763 JAEGER, M. J. & OTIS, A. B. (1964) Journal of Applied Physiology 19, 83-91 LEITH, D. E. & GILLESPIE, J. R. (1971) Federation Proceedings 30,551 LEKEUX, P., ART, T., CLERCX, C, GUSTIN, P. (1988) Veterinary Research Communications 12, 61-66 McILROY, M. B., MARSHALL, R. & CHRISTIE, R. V. (1954) Clinical Sciences 13, 127-136 MANOHAR, M. (1986) American Journal of Veterinary Research 47,1387-1394 MARGARIA, R., MILlC-EMILI, G., PETIT, J. M. & CAVAGNA, G. (1960) Journal of Applied Physiology 15, 354-358 MEAD, J. (1956) Journal of Applied Physiology 9, 208-212 MEAD, J. (1960) Journal of Applied Physiology 15, 325-336 MILlC-EMILI, G., MEAD, J. & TURNER, J. M. (1964) Journal of Applied Physiology 19, 212-216
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Received October /4, 1987 Accepted February 7, 1988