Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Respiratory Muscle Energetics

Charis Roussos, E. J. M. Campbell

10.1002/cphy.cp030328

Source: Supplement 12: Handbook of Physiology, The Respiratory System, Mechanics of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Thermodynamics
1.1 Heat, Work, and Efficiency
1.2 Energy Balance
1.3 Energetics and Limitation of Airflow
2 Energy Supply
2.1 Blood Flow
2.2 Substrate Metabolism
2.3 Estimation of Energy Change
2.4 Tension‐Time Index
3 Work of Breathing
3.1 Definitions
3.2 Positive Work, Negative Work, and No Work
3.3 Graphical Analysis of Work
3.4 Theoretical Estimation of Work
3.5 Measurement of Mechanical Work
3.6 Work Rate (Power)
3.7 Maximal Available Work and Power
4 Efficiency of Breathing
4.1 Mechanical Work
4.2 Metabolic Cost
5 Physiological Considerations
5.1 Optimal Breathing Frequency
5.2 Respiratory Muscle Energetics and Exercise
5.3 Respiratory Muscle Energetics in Health and Disease
Figure 1. Figure 1.

Variation of energy production (top) and efficiency (middle) during muscle twitches at different shortening velocities. Curve 1, total energy as function of velocity of fiber shortening; curve 2, heat production, which is composed of heat of shortening (curve 3), heat of activation, and heat of tension and duration [f(P,t)], which is the difference between curves 2 and 3. Energy production is greatest at velocity where greatest amount of work is done (Fenn effect). Interpretation of heat production (bottom) depicts time spent shortening (curve 5) and distance (x) shortened (curve 4). Q, heat; W, work; ax, heat of shortening; E, efficiency.

From Mommaerts 92
Figure 2. Figure 2.

Blood flow to respiratory muscles during inspiratory (A) and expiratory (B) loaded breathing. Note marked increase of diaphragmatic blood flow with increased rate of work of breathing. Transverse abdominal receives largest amount of blood flow at comparable rates of work done on the lung (e.g., 2 cal/min).

From Robertson et al. 106
Figure 3. Figure 3.

For similar rates of work performed on the lung, expiratory resistance requires a significantly greater total blood flow to respiratory muscles than either inspiratory resistance or hyperventilation induced by CO2 rebreathing.

From Robertson et al. 107
Figure 4. Figure 4.

Blood flow to respiratory muscles during low cardiac output (30% of control) in spontaneously breathing (SB) or mechanically ventilated (Mv) dogs. A: respiratory blood flow expressed in percent change from values obtained during quiet breathing (control) with normal circulation (horizontal dotted line). B: respiratory blood flow expressed in percent of cardiac output. Note large amount of respiratory blood flow during SB, amounting to 20% cardiac output compared with 3% of cardiac output during Mv.

From Viires et al. 126
Figure 5. Figure 5.

Blood lactate levels in 2 groups of dogs submitted to low cardiac output. Spontaneously breathing dogs had greater blood lactate concentration than the paralyzed and mechanically ventilated dogs.

From Aubier et al. 11
Figure 6. Figure 6.

Oxygen cost of breathing at various levels of ventilation. Ventilation is increased either by breathing through a dead space or voluntarily (administering CO2 to avoid hypocapnia). Note variability among studies and steep slope of patients with emphysema.

From Roussos 118
Figure 7. Figure 7.

Pressure‐volume diagram in terms of pleural pressure (left) and mouth pressure (right). Horizontal hatching, elastic work done by inspiratory muscles during inspiration.

From Roussos 118
Figure 8. Figure 8.

Pressure‐volume diagram in terms of pleural pressure (left) and pleural and mouth pressure (right). Horizontal hatching, elastic work done by inspiratory muscles during inspiration.

From Roussos 118
Figure 9. Figure 9.

Pressure‐volume diagram in terms of pleural pressure (left), pleural and mouth pressure (middle), and mouth pressure (right). Horizontal hatching, inspiratory elastic work; vertical hatching, inspiratory work required to overcome flow resistance of the lung (airways and tissue); oblique hatching, inspiratory work required to overcome flow resistance of the chest wall; cross‐hatching, inspiratory work required to overcome the flow resistance of the lung and chest wall.

From Roussos 118
Figure 10. Figure 10.

Pressure‐volume diagram in terms of pleural pressure (left) and mouth pressure (right). Horizontal hatching, negative work performed by inspiratory muscles during expiration; areas a and b, energy stored in the lung during inspiration and dissipated during expiration to overcome flow resistances of lung and chest wall, respectively (their sum equals area c).

From Roussos 118
Figure 11. Figure 11.

Graphical analysis of work done during a breathing cycle at increased ventilation. Cycle starts at resting volume of respiratory system. A: vertical hatching, work done by inspiratory muscles to overcome flow resistance of the lung; horizontal hatching, work done by inspiratory muscles to overcome elastic resistance of the lung; cross hatching, work done by inspiratory muscles to overcome elastic resistance of the chest wall; oblique hatching, work done by inspiratory muscles to overcome flow resistance of the chest wall; coarse stippling, elastic energy transferred from the chest wall to the lung. B: horizontal and cross hatching, work done by elastic energy of the lung and chest wall, respectively, against persistent activity of inspiratory muscles; fine stippling, work done by elastic energy of the lung to overcome part of flow resistance of the lung; broken hatching, work done by expiratory muscles to overcome rest of flow resistance of the lung (according to representation used; but this energy could be utilized to overcome part of the flow resistance of the chest wall); oblique hatching and solid area, work done by elastic energy of the lung and chest wall, respectively, to overcome flow resistance of the chest wall; coarse stippling, elastic energy transferred from the lung to the chest wall.

From Campbell et al. 24
Figure 12. Figure 12.

Graphical analysis of work done during a breathing cycle at increased ventilation. Cycle starts below resting volume of respiratory system. A: broken hatching, work done by elastic energy of the chest wall to overcome persistent activity of expiratory muscles; fine stippling, work done by elastic energy of the chest wall to overcome part of flow resistance of the lung (gas and tissues); area with small crosses, work done by elastic energy of the chest wall to overcome part of flow resistance of the chest wall; oblique hatching, work done by inspiratory muscles to overcome rest of flow resistance of the chest wall; vertical hatching, work done by inspiratory muscles to overcome part of flow resistance of the lung; horizontal hatching, work done by inspiratory muscles to overcome elastic resistance of the lung; coarse stippling, elastic energy transferred from the chest wall to the lung. B: horizontal hatching, work done by elastic energy of the lung against persistent activity of inspiratory muscles; fine stippling, work done by elastic energy of the lung to overcome part of flow resistance of the lung; oblique hatching, work done by elastic energy of the lung to overcome part of flow resistance of the lung; oblique hatching, work done by elastic energy of the lung to overcome part of flow resistance of the chest wall; vertical broken hatching, work done by expiratory muscles to overcome part of flow resistance of the chest wall; oblique broken hatching, work done by expiratory muscles to overcome part of flow resistance of the lung; horizontal broken hatching, work done by expiratory muscles to overcome elastic resistance of the chest wall; coarse stippling, elastic energy transferred from the lung to the chest wall.

From Campbell et al. 24
Figure 13. Figure 13.

Pressure‐volume relationship of respiratory system during breathing cycles at various lung volumes. Various types of work and total mechanical work can be analyzed as:

Cycle

Elastic Work

Flow‐Resistive Work

Negative Work

Total Mechanical Work for One Breathing Cycle

a

ABCA

AICA

BCEAB

AICBA + BCEAB

b

ABCA

AICA + BEAB

AICBEA

c

ABCA

AICA + DEAD

BCDB

AICBDEA + BCDB

d

ABCDA

DICD

BCEDAB

ADICBA + BCEDAB

e

BADCB

CEDC

ADICBA

BCEDAB + ADICBA

f

RBCR + RADR

QICRQ + PEDRP

BCPB + ADQA

DAQICBPED + BCPB + ADQA

From Otis 130.
Figure 14. Figure 14.

Pressure‐volume diagram (Campbell diagram). Top: lung volume (left ordinate) and rib cage volume (right ordinate) vs. transthoracic pressure. Bottom: abdominal volume (right ordinate) vs. transthoracic pressure. For details see text.

From Goldman et al. 50
Figure 15. Figure 15.

Relationship between rate of mechanical work of breathing and minute ventilation during muscular exercise of various intensities. Solid line indicates 25% greater rate of work of breathing found by Goldman et al. 50, who calculated changes of rib cage and abdominal volume instead of measuring changes of lung volumes at the mouth.

From Roussos 118
Figure 16. Figure 16.

Mechanical work of breathing as a function of frequency of breathing. A: frequency at which minimal work occurs at several constant rates of alveolar ventilation (). Note that frequency for minimal work increases progressively with increased . Open circles, frequencies spontaneously chosen by subjects during exercise and corresponding closely at each level of with frequency resulting in minimal work. B: contribution of elastic and turbulent work to total work of breathing at constant and dead space (VDS). Note that as frequency increases, elastic work decreases and reaches a plateau, whereas viscous and turbulent work increase.

A from Milic‐Emili and Petit 87; B from Otis et al. 99
Figure 17. Figure 17.

Energy expenditure per volume (dU/dV) as a function of minute ventilation () in 2 subjects. Solid lines (dUT/dV), slope of curve between total energy uptake (UT) and ventilation (); broken lines (dUrs/dV), slopes of curve between energy consumption of respiratory system (Urs) and ventilation at different values of mechanical efficiency (0.05, 0.10, 0.20, and 0.25).

From Margaria et al. 75
Figure 18. Figure 18.

Effects of respiratory muscle energetic requirements of humans in health and disease. Upper quadrant: relationship between respiratory muscle energy expenditure and power output at different levels of efficiency (1%, 2%, 3%, 5%, 10%, and 20%). N, value obtained during hyperventilation in normal subjects in upright position; P, value obtained from normal breathing through resistance or subjects with airflow limitation. [Data from McGregor and Becklake 79.] Lower quadrant: respiratory muscle power output as a function of ventilation by varying constants a and b.

Data from Milic‐Emili et al. 90


Figure 1.

Variation of energy production (top) and efficiency (middle) during muscle twitches at different shortening velocities. Curve 1, total energy as function of velocity of fiber shortening; curve 2, heat production, which is composed of heat of shortening (curve 3), heat of activation, and heat of tension and duration [f(P,t)], which is the difference between curves 2 and 3. Energy production is greatest at velocity where greatest amount of work is done (Fenn effect). Interpretation of heat production (bottom) depicts time spent shortening (curve 5) and distance (x) shortened (curve 4). Q, heat; W, work; ax, heat of shortening; E, efficiency.

From Mommaerts 92


Figure 2.

Blood flow to respiratory muscles during inspiratory (A) and expiratory (B) loaded breathing. Note marked increase of diaphragmatic blood flow with increased rate of work of breathing. Transverse abdominal receives largest amount of blood flow at comparable rates of work done on the lung (e.g., 2 cal/min).

From Robertson et al. 106


Figure 3.

For similar rates of work performed on the lung, expiratory resistance requires a significantly greater total blood flow to respiratory muscles than either inspiratory resistance or hyperventilation induced by CO2 rebreathing.

From Robertson et al. 107


Figure 4.

Blood flow to respiratory muscles during low cardiac output (30% of control) in spontaneously breathing (SB) or mechanically ventilated (Mv) dogs. A: respiratory blood flow expressed in percent change from values obtained during quiet breathing (control) with normal circulation (horizontal dotted line). B: respiratory blood flow expressed in percent of cardiac output. Note large amount of respiratory blood flow during SB, amounting to 20% cardiac output compared with 3% of cardiac output during Mv.

From Viires et al. 126


Figure 5.

Blood lactate levels in 2 groups of dogs submitted to low cardiac output. Spontaneously breathing dogs had greater blood lactate concentration than the paralyzed and mechanically ventilated dogs.

From Aubier et al. 11


Figure 6.

Oxygen cost of breathing at various levels of ventilation. Ventilation is increased either by breathing through a dead space or voluntarily (administering CO2 to avoid hypocapnia). Note variability among studies and steep slope of patients with emphysema.

From Roussos 118


Figure 7.

Pressure‐volume diagram in terms of pleural pressure (left) and mouth pressure (right). Horizontal hatching, elastic work done by inspiratory muscles during inspiration.

From Roussos 118


Figure 8.

Pressure‐volume diagram in terms of pleural pressure (left) and pleural and mouth pressure (right). Horizontal hatching, elastic work done by inspiratory muscles during inspiration.

From Roussos 118


Figure 9.

Pressure‐volume diagram in terms of pleural pressure (left), pleural and mouth pressure (middle), and mouth pressure (right). Horizontal hatching, inspiratory elastic work; vertical hatching, inspiratory work required to overcome flow resistance of the lung (airways and tissue); oblique hatching, inspiratory work required to overcome flow resistance of the chest wall; cross‐hatching, inspiratory work required to overcome the flow resistance of the lung and chest wall.

From Roussos 118


Figure 10.

Pressure‐volume diagram in terms of pleural pressure (left) and mouth pressure (right). Horizontal hatching, negative work performed by inspiratory muscles during expiration; areas a and b, energy stored in the lung during inspiration and dissipated during expiration to overcome flow resistances of lung and chest wall, respectively (their sum equals area c).

From Roussos 118


Figure 11.

Graphical analysis of work done during a breathing cycle at increased ventilation. Cycle starts at resting volume of respiratory system. A: vertical hatching, work done by inspiratory muscles to overcome flow resistance of the lung; horizontal hatching, work done by inspiratory muscles to overcome elastic resistance of the lung; cross hatching, work done by inspiratory muscles to overcome elastic resistance of the chest wall; oblique hatching, work done by inspiratory muscles to overcome flow resistance of the chest wall; coarse stippling, elastic energy transferred from the chest wall to the lung. B: horizontal and cross hatching, work done by elastic energy of the lung and chest wall, respectively, against persistent activity of inspiratory muscles; fine stippling, work done by elastic energy of the lung to overcome part of flow resistance of the lung; broken hatching, work done by expiratory muscles to overcome rest of flow resistance of the lung (according to representation used; but this energy could be utilized to overcome part of the flow resistance of the chest wall); oblique hatching and solid area, work done by elastic energy of the lung and chest wall, respectively, to overcome flow resistance of the chest wall; coarse stippling, elastic energy transferred from the lung to the chest wall.

From Campbell et al. 24


Figure 12.

Graphical analysis of work done during a breathing cycle at increased ventilation. Cycle starts below resting volume of respiratory system. A: broken hatching, work done by elastic energy of the chest wall to overcome persistent activity of expiratory muscles; fine stippling, work done by elastic energy of the chest wall to overcome part of flow resistance of the lung (gas and tissues); area with small crosses, work done by elastic energy of the chest wall to overcome part of flow resistance of the chest wall; oblique hatching, work done by inspiratory muscles to overcome rest of flow resistance of the chest wall; vertical hatching, work done by inspiratory muscles to overcome part of flow resistance of the lung; horizontal hatching, work done by inspiratory muscles to overcome elastic resistance of the lung; coarse stippling, elastic energy transferred from the chest wall to the lung. B: horizontal hatching, work done by elastic energy of the lung against persistent activity of inspiratory muscles; fine stippling, work done by elastic energy of the lung to overcome part of flow resistance of the lung; oblique hatching, work done by elastic energy of the lung to overcome part of flow resistance of the lung; oblique hatching, work done by elastic energy of the lung to overcome part of flow resistance of the chest wall; vertical broken hatching, work done by expiratory muscles to overcome part of flow resistance of the chest wall; oblique broken hatching, work done by expiratory muscles to overcome part of flow resistance of the lung; horizontal broken hatching, work done by expiratory muscles to overcome elastic resistance of the chest wall; coarse stippling, elastic energy transferred from the lung to the chest wall.

From Campbell et al. 24


Figure 13.

Pressure‐volume relationship of respiratory system during breathing cycles at various lung volumes. Various types of work and total mechanical work can be analyzed as:

Cycle

Elastic Work

Flow‐Resistive Work

Negative Work

Total Mechanical Work for One Breathing Cycle

a

ABCA

AICA

BCEAB

AICBA + BCEAB

b

ABCA

AICA + BEAB

AICBEA

c

ABCA

AICA + DEAD

BCDB

AICBDEA + BCDB

d

ABCDA

DICD

BCEDAB

ADICBA + BCEDAB

e

BADCB

CEDC

ADICBA

BCEDAB + ADICBA

f

RBCR + RADR

QICRQ + PEDRP

BCPB + ADQA

DAQICBPED + BCPB + ADQA

From Otis 130.



Figure 14.

Pressure‐volume diagram (Campbell diagram). Top: lung volume (left ordinate) and rib cage volume (right ordinate) vs. transthoracic pressure. Bottom: abdominal volume (right ordinate) vs. transthoracic pressure. For details see text.

From Goldman et al. 50


Figure 15.

Relationship between rate of mechanical work of breathing and minute ventilation during muscular exercise of various intensities. Solid line indicates 25% greater rate of work of breathing found by Goldman et al. 50, who calculated changes of rib cage and abdominal volume instead of measuring changes of lung volumes at the mouth.

From Roussos 118


Figure 16.

Mechanical work of breathing as a function of frequency of breathing. A: frequency at which minimal work occurs at several constant rates of alveolar ventilation (). Note that frequency for minimal work increases progressively with increased . Open circles, frequencies spontaneously chosen by subjects during exercise and corresponding closely at each level of with frequency resulting in minimal work. B: contribution of elastic and turbulent work to total work of breathing at constant and dead space (VDS). Note that as frequency increases, elastic work decreases and reaches a plateau, whereas viscous and turbulent work increase.

A from Milic‐Emili and Petit 87; B from Otis et al. 99


Figure 17.

Energy expenditure per volume (dU/dV) as a function of minute ventilation () in 2 subjects. Solid lines (dUT/dV), slope of curve between total energy uptake (UT) and ventilation (); broken lines (dUrs/dV), slopes of curve between energy consumption of respiratory system (Urs) and ventilation at different values of mechanical efficiency (0.05, 0.10, 0.20, and 0.25).

From Margaria et al. 75


Figure 18.

Effects of respiratory muscle energetic requirements of humans in health and disease. Upper quadrant: relationship between respiratory muscle energy expenditure and power output at different levels of efficiency (1%, 2%, 3%, 5%, 10%, and 20%). N, value obtained during hyperventilation in normal subjects in upright position; P, value obtained from normal breathing through resistance or subjects with airflow limitation. [Data from McGregor and Becklake 79.] Lower quadrant: respiratory muscle power output as a function of ventilation by varying constants a and b.

Data from Milic‐Emili et al. 90
References
 1. Adachi, H., W. Straus, H. Ochi, and H. N. Wagner, Jr. The effect of hypoxia on the regional distribution of cardiac output in the dog. Circ. Res. 29: 314–319, 1976.
 2. Agostoni, E., and W. O. Fenn. Velocity of muscle shortening as a limiting factor in respiratory air flow. J. Appl. Physiol. 15: 349–353, 1960.
 3. Agostoni, E., and P. Mognoni. Deformation of the chest wall during breathing efforts. J. Appl. Physiol. 21: 1827–1832, 1966.
 4. Agostoni, E., P. Mognoni, G. Torri, and G. Miserocchi. Forces deforming the rib cage. Respir. Physiol. 2: 105–117, 1966.
 5. Agostoni, E., P. Mognoni, G. Torri, and F. Saracino. Relation between changes of rib cage circumference and lung volume. J. Appl. Physiol 20: 1179–1186, 1965.
 6. Agostoni, E., F. F. Thimm, and W. O. Fenn. Comparative features of breathing. J. Appl. Physiol. 14: 679–683, 1959.
 7. Agostoni, E., and G. Torri. An analysis of the chest wall motions at high values of ventilation. Respir. Physiol. 3: 318–322, 1967.
 8. Aguggini, G., P. Mognoni, F. Saibene, and M. G. Clement. Flusso ematico nell'arteria diafragmatica di cane durante iperventilazione (Abstract). Atti Congr. Naz. Soc. It. Fisiol., 24th, Rome, 1972.
 9. Anrep, G. V., S. Cerqua, and A. Samaan. The effect of muscular contraction upon the blood flow in the skeletal muscle in the diaphragm and in the small intestine. Proc. R. Soc. London Ser. B 114: 245–257, 1933.
 10. Aubier, M., T. Trippenbach, and C. Roussos. Respiratory muscle fatigue during cardiogenic shock. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 499–508, 1981.
 11. Aubier, M., N. Viires, G. Sillye, and C. Roussos. Respiratory muscle contribution to lactic acidosis in low cardiac output. Am. Rev. Respir. Dis. 126: 648–652, 1982.
 12. Bartlett, R. G., Jr., H. F. Brubach, and H. Specht. Oxygen cost of breathing. J. Appl. Physiol. 12: 413–434, 1958.
 13. Bellemare, F., D. Wight, C. M. Lavigne, and A. Grassino. Effect of tension and timing of contraction on the blood flow of the diaphragm. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 54: 1597–1606, 1983.
 14. Benedict, F. A probable respiration apparatus for clinical use. Boston Med. Surg. J. 178: 667–678, 1918.
 15. Bergofsky, E. H. Relative contributions of the rib cage and the diaphragm to ventilation in man. J. Appl. Physiol. 19: 698–706, 1964.
 16. Bergofsky, E. H., G. M. Turino, and A. P. Fishman. Cardiorespiratory failure in kyphoscoliosis. Medicine Baltimore 38: 263–317, 1959.
 17. Bradley, M. E., and D. E. Leith. Ventilatory muscle training and the oxygen cost of sustained hyperpnea. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 45: 885–892, 1978.
 18. Buchler, B., S. Magder, H. Katsardis, Y. Jammes, and C. Roussos. Effects of pleural pressure and abdominal pressure on diaphragmatic blood flow. J. Appl. Physiol. 58: 691–697, 1985.
 19. Buchler, B., S. Magder, and C. Roussos. Effects of contraction frequency and duty cycle on diaphragmatic blood flow. J. Appl. Physiol. 58: 265–273, 1985.
 20. Buhlman, A., and H. Behn. Klinische Ergebnisse atemmechanischer Untersuchungen. Schweiz. Med. Wochenschr. 87: 1500–1509, 1957.
 21. Busse, J. Blood Flow and Metabolism of the Diaphragm of Intact Dogs. Cologne, West Germany: University of Cologne, 1977.
 22. Cain, C. C., and A. B. Otis. Some physiological effects resulting from added resistance to respiration. J. Aviat. Med. 20: 149–160, 1949.
 23. Campbell, E. J. M. The Respiratory Muscles and the Mechanics of Breathing. Chicago, IL: Year Book, 1958.
 24. Campbell, E. J. M., E. Agostoni, and J. Newsom Davis The Respiratory Muscles: Mechanics and Neural Control. Philadelphia, PA: Saunders, 1970.
 25. Campbell, E. J. M., E. K. Westlake, and R. M. Cherniack. Simple methods of estimating oxygen consumption and efficiency of the muscles of breathing. J. Appl. Physiol. 11: 303–308, 1957.
 26. Campbell, E. J. M., E. K. Westlake, and R. M. Cherniack. The oxygen consumption and efficiency of the respiratory muscles of young male subjects. Clin. Sci. 18: 55–64, 1958.
 27. Cavagna, G. A., and M. Kaneko. Mechanical work and efficiency in level walking and running. J. Physiol. London 26: 467–481, 1977.
 28. Cherniack, R. M. The oxygen consumption and efficiency of respiratory muscle in health and emphysema. J. Clin. Invest. 38: 494–499, 1959.
 29. Clark, J. M., R. D. Sinclair, and J. B. Lenox. Chemical and nonchemical components of ventilation during hypercapnic exercise in man. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 48: 1065–1076, 1980.
 30. Cook, C. D., J. M. Sutherland, S. Segal, R. B. Cherry, J. Mead, M. B. McIlroy, and C. A. Smith. Studies of respiratory physiology. III. Measurements of mechanics of respiration. J. Clin. Invest. 36: 440–448, 1957.
 31. Cooper, E. A. A comparison of the respiratory work done against an external resistance by man and by a sine wave pump. Q. J. Exp. Physiol 45: 179–191, 1960.
 32. Cournand, A., D. W. Richards, R. A. Bader, M. E. Bader, and A. P. Fishman. The oxygen cost of breathing. Trans. Assoc. Am. Physicians 67: 162–173, 1954.
 33. Craig, A. B., Jr. Maximal work of one breathing cycle. J. Appl. Physiol. 15: 1098–1100, 1960.
 34. Crosfill, M. L., and J. G. Widdicombe. Physical characteristics of the chest and lungs and the work of breathing in different mammalian species. J. Physiol London 158: 1–14, 1961.
 35. Curtin, N. A., and R. C. Woledge. Energy changes and muscular contraction. Physiol. Rev. 58: 690–761, 1978.
 36. Donovan, E., T. Trippenbach, A. Grassino, P. T. Macklem, and C. Roussos. Effect of isometric diaphragmatic contraction on cardiac output and muscle blood flow (Abstract). Physiologist 22 ( 4): 30, 1979.
 37. DuBois, A. B., A. W. Brody, D. H. Lewis, and B. F. Burgess, Jr. Oscillation mechanics of lungs and chest in man. J. Appl Physiol. 8: 587–594, 1956.
 38. Eldridge, F. Anaerobic metabolism of the respiratory muscles. J. Appl. Physiol. 21: 853–857, 1966.
 39. Evans, C. L., and A. V. Hill. The relations of length to tension development and heat production on contraction in muscle. J. Physiol. London 49: 1–16, 1914.
 40. Fenn, W. O. A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J. Physiol. London 58: 175–203, 1923.
 41. Fenn, W. O. The relation between the work performed and the energy liberated in muscle contraction. J. Physiol. London 58: 373–395, 1924.
 42. Fenn, W. O. A comparison of respiratory and skeletal muscles. In: Perspectives in Biology, edited by C. F. Cori, V. G. Fogeia, L. F. Leboiv, and S. Ochoa Amsterdam: Elsevier, 1973, p. 293–300.
 43. Fenn, W. O., and B. S. Marsh. Muscular force at different speeds of shortening. J. Physiol. London 85: 277–297, 1935.
 44. Fixler, D. E., J. M. Atkins, J. H. Mitchell, and L. D. Horwitz. Blood flow to respiratory, cardiac, and limb muscles in dogs during graded exercise. Am. J. Physiol. 231: 1515–1519, 1976.
 45. Fritts, H. N., Jr., J. Filler, A. P. Fishman, and A. Cournand. The efficiency of ventilation during voluntary hyperpnea. J. Clin. Invest. 38: 1339–1348, 1959.
 46. Gibbs, C. L. Cardiac energetics. In: Mammalian Myocardium, edited by G. A. Langer and A. J. Brady New York: Wiley, 1974, p. 105–133.
 47. Gibbs, C. L. Cardiac energetics. Physiol. Rev. 58: 174–254, 1978.
 48. Gibbs, C. L., and J. B. Chapman. Cardiac energetics. In: Handbook of Physiology. The Cardiovascular System, edited by R. M. Berne and N. Sperelakis Bethesda, MD: Am. Physiol. Soc., 1979, sect. 2, vol. I, chapt. 22, p. 775–804.
 49. Goldman, M. D. Thoracoabdominal Mechanics and the Work of Breathing. Boston, MA: Harvard School of Public Health, 1972.
 50. Goldman, M. D., G. Grimby, and J. Mead. Mechanical work of breathing derived from rib cage and abdominal V‐P partitioning. J. Appl. Physiol. 41: 752–763, 1976.
 51. Grimby, G., J. Bunn, and J. Mead. Relative contribution of rib cage and abdomen to ventilation during exercise. J. Appl. Physiol. 24: 159–166, 1968.
 52. Grimby, G., M. Goldman, and J. Mead. Respiratory muscle action inferred from rib cage and abdominal V‐P partitioning. J. Appl. Physiol. 41: 739–751, 1976.
 53. Hales, J. R. S. Effects of heat stress on blood flow in respiratory and non‐respiratory muscle in the sheep. Pfluegers Arch. 345: 123–130, 1973.
 54. Hill, A. V. Length of muscle and the heat and tension developed in an isometric contraction. J. Physiol. London 60: 237–263, 1925.
 55. Hill, A. V. The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. London Ser. B 126: 136–195, 1938.
 56. Hill, A. V. The variation of total heat production in a twitch with velocity of shortening. Proc. R. Soc. London Ser. B 159: 596–605, 1964.
 57. Hollanders, F. D. The production of lactic acid by the diaphragm. Comp. Biochem. Physiol. 26: 907–916, 1968.
 58. Homsher, E., and C. J. Kean. Skeletal muscle energetics and metabolism. Annu. Rev. Physiol. 40: 93–131, 1978.
 59. Honig, C. R., and C. L. Odoroff. Calculated dispersion of capillary transit times: significance for oxygen exchange. Am. J. Physiol. 240 (Heart Circ. Physiol. 9): H199–H208, 1981.
 60. Horstman, D. H., M. Gleser, and J. Delehunt. Effects of altering O2 delivery on O2 of isolated, working muscle. Am. J. Physiol. 230: 327–334, 1976.
 61. jaeger, M. J. Verbessertes Verfahren zur Bestimmung des Alveolardruckes mit der Verschlussdruckmethode. Schweiz. Med. Wochschr. 92: 67–72, 1962.
 62. Jaeger, M. J., and A. B. Otis. Effects of compressibility of alveolar gas on dynamics and work of breathing. J. Appl. Physiol. 19: 83–91, 1964.
 63. Jammes, Y., P. T. P. Bye, R. L. Pardy, and C. Roussos. Vagal feedback with expiratory threshold load under extracorporeal circulation. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 55: 316–322, 1983.
 64. Jardim, J., G. Farkas, C. Prefaut, D. Thomas, P. T. Macklem, and C. Roussos. The failing inspiratory muscles under normoxic and hypoxic conditions. Am. Rev. Respir. Dis. 124: 274–279, 1981.
 65. Kety, S. S., and C. F. Schmidt. The determination of cerebral blood flow in man by the use of nitrous oxide in low concentrations. Am. J. Physiol. 143: 53–66, 1945.
 66. Konno, K., and J. Mead. Static volume‐pressure characteristics of the rib cage and abdomen. J. Appl. Physiol. 24: 544–548, 1968.
 67. Laughlin, M. H., and R. B. Armstrong. Muscular blood flow distribution patterns as a function of running speed in rats. Am. J. Physiol. 243 (Heart Circ. Physiol. 12): H296–H306, 1982.
 68. Liljestrand, G. Untersuchungen über die Atmungsarbeit. Skand. Arch. Physiol. 35: 199–293, 1918.
 69. Loring, S. H., and J. Mead. Action of the diaphragm on the rib cage inferred from a force‐balance analysis. J. Appl. Physiok: Respirat. Environ. Exercise Physiol. 53: 756–760, 1982.
 70. Macklem, P. T. A mathematical and graphical analysis of inspiratory muscles action. Respir. Physiol. 38: 133–171, 1979.
 71. Macklem, P. T., D. Gross, A. Grassino, C. Roussos. Partitioning of inspiratory pressure swings between diaphragm and intercostal/accessory muscles. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 44: 200–208, 1978.
 72. Macklem, P. T., D. M. Macklem, and A. De Troyer. A model of inspiratory muscles mechanics. J. Appl Physiol.: Respirat. Environ. Exercise Physiol. 55: 547–557, 1983.
 73. Macklem, P. T., C. Roussos, J. P. Derenne, and L. Delhez. The interaction between the diaphragm intercostal/accessory muscles of inspiration and the rib cage. Respir. Physiol. 38: 141–152, 1979.
 74. Manohar, M., J. Thurmon, W. J. Tranquilli, M. Devous, M. Theodovakis, R. Shawley, D. Feller, and J. Benson. Regional myocardial blood flow and coronary vascular reserve in unanesthetized young calves with severe concentric right ventricular hypertrophy. Circ. Res. 48: 785–796, 1981.
 75. Margaria, R., G. Milic‐Emili, J. M. Petit, and G. Cavagna. Mechanical work of breathing during muscular exercise. J. Appl. Physiol. 15: 354–358, 1960.
 76. McDonald, R. H., Jr. Developed tension: a major determinant of myocardial oxygen consumption. Am. J. Physiol. 210: 351–356, 1966.
 77. McGilvery, R. W. The use of fuels for muscular work. In: Metabolic Adaptation to Prolonged Physical Exercise, edited by H. Howald and J. R. Poortmans Berlin: Birkhäuser, 1975, p. 12–30.
 78. McGilvery, R. W. Fuel for breathing. Am. Rev. Respir. Dis. 119: 85–88, 1979.
 79. McGregor, M., and M. Becklake. The relationship of oxygen cost of breathing to respiratory mechanical work and respiratory force. J. Clin. Invest. 40: 971–980, 1961.
 80. McIlroy, M. R., R. Marshall, and R. V. Christie. Work of breathing in normal subjects. Clin. Sci. 13: 127–136, 1954.
 81. McKerrow, C. B., and A. B. Otis. Oxygen cost of hyperventilation. J. Appl. Physiol. 9: 375–379, 1956.
 82. Mead, J. Measurement of inertia of the lungs at increased ambient pressure. J. Appl. Physiol. 9: 208–212, 1956.
 83. Mead, J. Control of respiratory frequency. J. Appl. Physiol. 15: 325–336, 1960.
 84. Mead, J., and S. H. Loring. Analysis of volume displacement and length changes of the diaphragm during breathing. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 53: 750–755, 1982.
 85. Mead, J., J. C. Smith, and S. H. Loring. Volume displacements of the chest wall and their mechanical significance. In: Lung Biology in Health and Disease. The Thorax, edited by C. Roussos and P. T. Macklem New York: Dekker, 1985, p. 369–392.
 86. Milic‐Emili, J., J. Mead, and J. M. Turner. Topography of esophageal pressure as a function of posture in man. J. Appl. Physiol. 19: 212–216, 1964.
 87. Milic‐Emili, G., and J. M. Petit. Il lavoro mecanico della respirazione a varia frequenza respiratoria. Arch. Sci. Biol. Bologna 43: 326–330, 1959.
 88. Milic‐Emili, G., and J. M. Petit. Mechanical efficiency of breathing. J. Appl. Physiol. 15: 359–362, 1960.
 89. Milic‐Emili, G., J. M. Petit, and R. Deroanne. The effects of respiratory rate on the mechanical work of breathing during muscular exercise. Int. Z. Angew. Physiol. Einschl. Arbeitsphysiol. 18: 330–340, 1960.
 90. Milic‐Emili, G., J. M. Petit, and R. Deroanne. Mechanical work of breathing during exercise in trained and untrained subjects. J. Appl. Physiol. 17: 43–46, 1962.
 91. Mognoni, P., F. Saibene, G. Sant'Ambrogio, and E. Camparesi. Perfusion of inspiratory muscles at different levels of ventilation in rabbits. Respir. Physiol. 20: 171–179, 1974.
 92. Mommaerts, W. F. H. M. Energetics of muscular contraction. Physiol. Rev. 49: 427–508, 1969.
 93. Monroe, R. G., R. H. Strang, C. G. LaFarge, and J. Levy. Ventricular performance, pressure‐volume relationships, and O2 consumption during hypothermia. Am. J. Physiol. 206: 67–73, 1964.
 94. Newhouse, M. T., M. R. Becklake, P. T. Macklem, and M. McGregor. Effect of alterations in end tidal CO2 tension on flow resistance. J. Appl. Physiol. 19: 745–749, 1964.
 95. Nielsen, M. Die Respirationsarbeit bei Körperruhe und bei Muskul Arbeit. Skand. Arch. Physiol. 74: 299–316, 1936.
 96. Odessey, R. Amino acid and protein metabolism in the diaphragm. Am. Rev. Respir. Dis. 119: 107–112, 1979.
 97. Opie, L. H., J. M. K. Splading, and F. D. Scott. Mechanical properties of the chest during intermittent positive‐pressure respiration. Lancet 1: 545–550, 1959.
 98. Otis, A. B. The work of breathing. Physiol. Rev. 34: 449–458, 1954.
 99. Otis, A. B. The work of breathing. In: Handbook of Physiology. Respiration, edited by W. O. Fenn and H. Rahn Washington, DC: Am. Physiol. Soc., 1964, sect. 3, vol. I, chapt. 17, p. 463–476.
 100. Otis, A. B., W. O. Fenn, and H. Rahn. The mechanics of breathing in man. J. Appl. Physiol. 2: 592–607, 1950.
 101. Piiper, J., P. E. Di Prampero, and P. Cerretelli. Oxygen debt and high‐energy phosphates in gastrocnemius muscle of the dog. Am. J. Physiol. 215: 523–531, 1968.
 102. Rayford, C. R., E. M. Khouri, and D. E. Gregg. Effect of excitement on coronary and systemic energetics in unanaesthetized dogs. Am. J. Physiol. 209: 680–688, 1965.
 103. Reid, M. B., and R. L. Johnson, Jr. Efficiency, maximal blood flow, and aerobic work capacity of canine diaphragm. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 54: 763–772, 1983.
 104. Remmers, J. E., and I. Marttila. Action of intercostal muscle afferents on the respiratory rhythm of anesthetized cats. Respir. Physiol. 24: 31–41, 1975.
 105. Riley, R. L. The work of breathing and its relation to respiratory acidosis. Ann. Intern. Med. 41: 172–176, 1954.
 106. Robertson, C. H., Jr., W. L. Eshenbacher, and R. L. Johnson, Jr. Respiratory muscle blood flow distribution during expiratory resistance. J. Clin. Invest. 60: 473–480, 1977.
 107. Robertson, C. H., Jr., G. H. Foster, and R. L. Johnson, Jr. The relationship of respiratory failure to the oxygen consumption of, lactic production by, and distribution of blood flow among respiratory muscles during increasing inspiratory resistance. J. Clin. Invest. 59: 31–42, 1977.
 108. Robertson, C. H., Jr., M. A. Pagel, and R. L. Johnson, Jr. The distribution of blood flow, oxygen consumption, and work output among the respiratory muscles during obstructed hyperventilation. J. Clin. Invest. 59: 43–50, 1977.
 109. Rochester, D. F. Measurement of diaphragmatic blood flow and oxygen consumption in the dog by the Kety‐Schmidt technique. J. Clin. Invest. 53: 1126–1221, 1974.
 110. Rochester, D. F., and G. Bettini. Diaphragmatic blood flow and energy expenditure in the dog. J. Clin. Invest. 57: 661–672, 1976.
 111. Rochester, D. F., and A. M. Briscoe. Metabolism of the working diaphragm. Am. Rev. Respir. Dis. 119: 85–88, 1979.
 112. Rochester, D. F., and M. Pradel‐Guena. Measurement of diaphragmatic blood flow in dogs from xenon 133 clearance. J. Appl. Physiol. 34: 68–74, 1973.
 113. Rohrer, F. Physiologie der Atembewegung. In: Handbuch der normalen und pathologischen Physiologie, edited by A. T. J. Bethe, G. von Bergmann, G. Embden, and A. Ellinger Berlin: Springer‐Verlag, 1925, vol. 2, p. 70–127.
 114. Roncoroni, A. J., H. J. A. Adrougué, C. W. De Obrutsky, M. L. Marchisio, and M. R. Herrero. Metabolic acidosis in status asthmaticus. Respiration 33: 85–94, 1976.
 115. Rossier, P. H., and A. Bühlmann. Dyspnoe und Atemarbeit. Schweiz. Med. Wochenschr. 89: 543–548, 1959.
 116. Roth, P. Graphic method for the estimation of the metabolic rate. Boston Med. Surg. J. 196: 457, 1922.
 117. Rous, P., and H. P. Gilding. Studies of tissue maintenance. I. The changes with diminished blood bulk. J. Exp. Med. 50: 189–211, 1929.
 118. Roussos, C. Limits to economics of respiratory muscles. Bull. Eur. Physiopathol. Respir. 18, Suppl. 4: 113–118, 1982.
 119. Roussos, C. Energetics. In: Lung Biobgy in Health and Disease. The Thorax, edited by C. Roussos and P. T. Macklem New York: Dekker, 1985, p. 437–492.
 120. Roussos, C. S., and P. T. Macklem. Diaphragmatic fatigue in man. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 43: 189–197, 1977.
 121. Roussos, C., and P. T. Macklem. The respiratory muscles. N. Engl. J. Med. 307: 786–797, 1982.
 122. Sarnoff, S. J., E. Braunwald, and G. H. Welch, Jr., R. B. Case, W. N. Stainsby, and R. Macurz. Hemodynamic determinants of oxygen consumption of the heart with special reference to the tension‐time index. Am. J. Physiol. 192: 148–156, 1958.
 123. Sharp, J., J. P. Henry, S. K. Sweany, W. R. Meadows, and R. J. Pietras. The total work of breathing in normal and obese men. J. Clin. Invest. 43: 728–739, 1964.
 124. Shephard, R. J. The oxygen cost of breathing during vigorous exercise. Q. J. Exp. Physiol. 57: 336–350, 1966.
 125. Sonnenblick, E. H., J. Ross, Jr., J. W. Covell, G. A. Kaiser, and E. Braunwald. Velocity of contraction as a determinant of myocardial oxygen consumption. Am. J. Physiol. 209: 919–927, 1965.
 126. Stainsby, W. N., and H. G. Welch. Lactate metabolism of contracting dog skeletal muscle in situ. Am. J. Physiol. 211: 177–183, 1966.
 127. Viires, N., G. Sillye, A. Aubier, G. Rassidakis, and C. Roussos. Regional blood flow distribution in dog during induced hypotension and low cardiac output. Spontaneous breathing versus artificial ventilation. J. Clin. Invest. 72: 935–947, 1983.
 128. Wilkie, D. R. The relation between force and velocity in human muscle. J. Physiol. London 110: 249–280, 1950.
 129. Wilkie, D. R. Heat work and phosphorylcreatine break‐down in muscle. J. Physiol. London 195: 157–183, 1968.
 130. Wilkie, D. R. The efficiency of muscular contraction. J. Mechanochem. Cell Motil. 2: 257–267, 1974.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Respiratory Muscle Energetics
 

How to Cite

Charis Roussos, E. J. M. Campbell. Respiratory Muscle Energetics. Compr Physiol 2011, Supplement 12: Handbook of Physiology, The Respiratory System, Mechanics of Breathing: 481-509. First published in print 1986. doi: 10.1002/cphy.cp030328