Comprehensive Physiology Wiley Online Library

Respiratory Muscle Energetics

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
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.
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.
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.
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.
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
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
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
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; crosshatching, inspiratory work required to overcome the flow resistance of the lung and chest wall.

From Roussos
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
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.
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.
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 .

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.
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. , who calculated changes of rib cage and abdominal volume instead of measuring changes of lung volumes at the mouth.

From Roussos
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 ; B from Otis et al.
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.
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 .] Lower quadrant: respiratory muscle power output as a function of ventilation by varying constants a and b.

Data from Milic‐Emili et al.


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


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.


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.


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.


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.


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


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


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


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; crosshatching, inspiratory work required to overcome the flow resistance of the lung and chest wall.

From Roussos


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


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.


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.


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 .



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.


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. , who calculated changes of rib cage and abdominal volume instead of measuring changes of lung volumes at the mouth.

From Roussos


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 ; B from Otis et al.


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.


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 .] Lower quadrant: respiratory muscle power output as a function of ventilation by varying constants a and b.

Data from Milic‐Emili et al.
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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