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Mechanics of the Respiratory Muscles

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Abstract

This article examines the mechanics of the muscles that drive expansion or contraction of the chest wall during breathing. The diaphragm is the main inspiratory muscle. When its muscle fibers are activated in isolation, they shorten, the dome of the diaphragm descends, pleural pressure (Ppl) falls, and abdominal pressure (Pab) rises. As a result, the ventral abdominal wall expands, but a large fraction of the rib cage contracts. Expansion of the rib cage during inspiration is produced by the external intercostals in the dorsal portion of the rostral interspaces, the intercartilaginous portion of the internal intercostals (the so‐called parasternal intercostals), and, in humans, the scalenes. By elevating the ribs and causing an additional fall in Ppl, these muscles not only help the diaphragm expand the chest wall and the lung, but they also increase the load on the diaphragm and reduce the shortening of the diaphragmatic muscle fibers. The capacity of the diaphragm to generate pressure is therefore enhanced. In contrast, during expiratory efforts, activation of the abdominal muscles produces a rise in Pab that leads to a cranial displacement of the diaphragm into the pleural cavity and a rise in Ppl. Concomitant activation of the internal interosseous intercostals in the caudal interspaces and the triangularis sterni during such efforts contracts the rib cage and helps the abdominal muscles deflate the lung. © 2011 American Physiological Society. Compr Physiol 1:1273‐1300, 2011.

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Figure 1. Figure 1.

Coronal section of the human chest wall at end expiration. The costal diaphragmatic fibers run mainly cranially from their insertions on the lower ribs and are directly apposed to the inner aspect of the lower rib cage (zone of apposition). Reproduced, with permission, from De Troyer A, Loring SH. Actions of the respiratory muscles. In: Roussos C, editor. The Thorax (2nd ed), Vol. 85. New York: Marcel Dekker, 1995, pp. 535‐563).

Figure 2. Figure 2.

Respiratory displacements of the rib cage. (A) diagram of a typical thoracic vertebra and a pair of ribs (viewed from above). Each rib articulates with both the body and the transverse process of the vertebra (closed circles) and is bound to it by strong ligaments (right). The motion of the rib, therefore, occurs primarily through a rotation around the axis defined by these articulations (solid line and double arrow‐head). (B) and (C) ventral and lateral views, respectively, of the rib at end expiration (solid lines) and end inspiration (dotted lines). When the rib becomes more horizontal in inspiration, the transverse (B) and the anteroposterior (C) diameter of the rib cage increase (small arrows), and the sternum is displaced ventrally (vertical line in C). Reproduced, with permission, from De Troyer A. Respiratory muscle function. In: Shoemaker WC, Ayres SM, Grenvik A, Holbrook PR, editors. Textbook of Critical Care. W.B. Saunders, 2000, pp. 1172‐1184).

Figure 3. Figure 3.

Mean ± SE changes in airway opening pressure (ΔPao) and abdominal pressure (ΔPab) obtained from six dogs during isolated, bilateral stimulation of the phrenic nerves at five different lung volumes from FRC (transrespiratory pressure = 0 cmH2O) to TLC (transrespiratory pressure = 30 cmH2O). All stimulations were performed while the endotracheal tube was occluded. The capacity of the diaphragm to generate pressure, in particular pleural pressure, decreases markedly with increasing lung volume. Reproduced, with permission, from ref. 49).

Figure 4. Figure 4.

Relationship between transdiaphragmatic pressure (Pdi) and diaphragm muscle length during isolated, supramaximal phrenic nerve stimulation at different lung volumes. The dashed line in the main panel is the aggregate relationship obtained for the costal and crural portions of the canine diaphragm in vivo by Road et al. 134, and the closed circles are the mean ± SE values obtained from six dogs (same animals as in Figure 3) during phrenic nerve stimulation at increasing lung volumes from FRC (top circle) to TLC (bottom circle). Muscle length was measured by computed tomography and is expressed as a percentage of muscle length during relaxation at FRC (LFRC). Note that the data point obtained at FRC is close to the length‐tension relationship of Road et al., but the data points obtained at high lung volumes lay well below the curve. Data in the inset are the mean values obtained before (closed circles) and after (open circle; bars, ± SE) bilateral pneumothorax in a subset of four animals. (Redrawn, with permission, from ref. 60).

Figure 5. Figure 5.

Graphical representation of the effect of inflation on the pressure developed by the diaphragm. The continuous lines are the Pdi‐length relationships for the maximally active and the passive diaphragm, and the dashed lines are the load lines describing the load imposed by the lung and chest wall on the diaphragm during isolated contraction at FRC and during isolated contraction at TLC. Pdi is expressed as a fraction of the maximal value, and muscle length is expressed as a fraction of optimal length (Lo). The pressure developed by the diaphragm during phrenic nerve stimulation at a given lung volume is given by the intersection (closed circle) of the load line with the maximally active Pdi‐length curve. Reproduced, with permission, from ref. 60).

Figure 6. Figure 6.

Graphical analysis of the pressure generated by the diaphragm in the presence of ascites. The continuous lines describing the Pdi‐length relationships for the maximally active and the passive diaphragm, and the dashed line describing the load line for the isolated diaphragm in the control condition are the same as those in Figure 5. The thin solid lines are the two load lines for the diaphragm in the presence of moderate and severe ascites. With moderate ascites, the relaxed diaphragm lengthens and the elastance of the abdomen increases, so that the load line is displaced upward and is more steep. As a result, the diaphragm during phrenic nerve stimulation shortens less and generates a larger pressure (closed triangle). With severe ascites, the load line is further displaced upward and still more steep, but the radius of diaphragm curvature during phrenic stimulation increases. Consequently, the active diaphragm is even longer, but the pressure generated (closed square) is smaller than anticipated on the basis of muscle length alone (open square).

Figure 7. Figure 7.

Contours of the diaphragm seen on anteroposterior radiographs in a dog during relaxation at FRC, during isolated tetanic stimulation of the right phrenic nerve (dashed line), and during combined stimulation of the left and right phrenic nerves. Stimulation frequency = 50 Hz. The two short bars on each contour correspond to the junctions of the muscle fibers with the central tendon and show the lateral shift of the tendon (and the mediastinum) during unilateral phrenic nerve stimulation. The surface area (volume) swept by the diaphragm during simultaneous contraction of the right and left hemidiaphragms is more than twice that swept when the right hemidiaphragm contracts in isolation.

Figure 8. Figure 8.

Diagram illustrating the actions of the intercostal muscles, as proposed by Hamberger 82. The two bars oriented obliquely in each panel represent two adjacent ribs. The external and internal (interosseous) intercostal muscles are depicted as single bundles, and the torques acting on the ribs during contraction of these muscles are represented by arrows. When the external intercostal contracts (A), the torque acting on the lower rib is greater than that acting on the upper rib; the opposite is true when the internal intercostal contracts (B). Reproduced, with permission, from ref. 45).

Figure 9. Figure 9.

Maximal respiratory effects of the canine external (A) and internal interosseous (B) intercostal muscles in the dorsal third, middle third, and ventral third of the even‐numbered interspaces (both sides of the sternum). The respiratory effects of the medial portion of the parasternal intercostals in interspaces 2, 4, 6, and 8 are also shown. Reproduced with permission from ref. 45).

Figure 10. Figure 10.

Effects of rib curvature on the net moment exerted by an intercostal muscle. (A) plan form of a typical rib in the dog and its axis of rotation (bold vector). At point a, the distances between the points of attachment of an intercostal muscle on the lower and upper ribs and the axes of rotation are different, and the muscle exerts a net moment on the ribs. At point b, however, the distances between the points of attachment of an intercostal muscle on the lower and upper ribs and the axes of rotation of the ribs are equal, and the muscle exerts no net moment. Thus the net moment exerted by the muscle depends on the angular position (θ) around the rib, as shown in (B). The external intercostal muscle (continuous line) has the greatest inspiratory moment in the dorsal portion of the rib cage (θ between 15 and 60°); this inspiratory moment then decreases as one moves around the rib cage (θ between 60 and 120°) and is reversed into an expiratory moment in the vicinity of the sternum (θ > 120°). The internal intercostal muscle (dashed line in B) shows a similar gradient in expiratory moment. Reproduced, with permission, from ref. 45).

Figure 11. Figure 11.

Effect on the lung of external loading of individual rib pairs in the cranial direction. Data are the mean ± SE values of the changes in airway opening pressure (ΔPao) per unit force (F) on the ribs obtained from seven animals. At FRC (closed circles), ΔPao /F increases from the second to the fifth rib pair and then decreases continuously to the eleventh rib pair. ΔPao /F for ribs 2 to 8, however, decreases markedly when lung volume is passively increased from FRC to 10 cmH2O (open circles) and 20 cmH2O (open triangles) transrespiratory pressure. Reproduced, with permission, from ref. 46.

Figure 12. Figure 12.

Patterns of rib displacement produced by the external and parasternal intercostals in the dog. In the animal in (A), the parasternal intercostals in interspaces 1 to 8 were denervated on both sides of the sternum; in the animal in (B), the parasternal intercostals were intact but the external intercostals in interspaces 1 to 8 were excised. Both animals had complete diaphragmatic paralysis. The dashed line in each panel is the trajectory of the ribs during passive inflation (relaxation), and the solid line with the arrowhead corresponds to a spontaneous inspiration. Reproduced, with permission, from ref. 58.

Figure 13. Figure 13.

Maximal inspiratory effects of the parasternal intercostal and external intercostal muscles in the even‐numbered interspaces in dogs (A) and in humans (B). Redrawn from ref 45, with permission.

Figure 14. Figure 14.

Effects of inflation on the pressure‐generating ability of the inspiratory intercostals. The closed circles are the mean ± SE values of ΔPao obtained from 19 dogs during isolated, tetanic stimulation of the inspiratory (and expiratory) intercostals at different lung volumes, as reported by DiMarco et al. 61. The open circles are the mean ± SE values of ΔPao obtained from 9 dogs during spontaneous contraction of the parasternal intercostals alone 102. Similar to the diaphragm, the pressure‐generating ability of the inspiratory intercostals decreases with increasing lung volume. Reproduced with permission from ref. 60.

Figure 15. Figure 15.

Dorsal view of the spine and one rib in its position at FRC and its position at 20 cmH2O transrespiratory pressure. Because the rib at FRC is slanted caudally, it moves both cranially (Xr) and outward (Yr) during cranial loading. However, at 20 cmH2O transrespiratory pressure, the rib is almost horizontal. Therefore, loading the rib causes a cranial displacement with little or no outward displacement. Reproduced with permission from ref. 46.

Figure 16. Figure 16.

Pattern of rib cage motion during mechanical ventilation (left) and during spontaneous breathing (right) in a quadriplegic subject with a traumatic transection of the upper cervical cord (C1). Each panel shows, from top to bottom, the respiratory changes in anteroposterior (AP) diameter of the lower rib cage, the changes in AP diameter of the upper rib cage, the changes in transverse diameter of the lower rib cage, and the changes in xiphi‐pubic distance. Upward deflections correspond to an increase in diameter or an increase in xiphi‐pubic distance (i.e., a cranial displacement of the sternum); I indicates the duration of inspiration. All rib cage diameters and the xiphi‐pubic distance increase in phase during mechanical inflation. When the sternomastoids contract forcefully during spontaneous inspiration, however, the xiphi‐pubic distance and the upper rib cage AP diameter increase proportionately more than the lower rib cage AP diameter, and the lower rib cage transverse diameter then decreases. Reproduced, with permission, from De Troyer A. Mechanics of the chest wall muscles. In: Miller AD, Bianchi AL, Bishop B, editors. Neural control of the respiratory muscles, CRC Press, Inc., 1996, pp. 59–73.



Figure 1.

Coronal section of the human chest wall at end expiration. The costal diaphragmatic fibers run mainly cranially from their insertions on the lower ribs and are directly apposed to the inner aspect of the lower rib cage (zone of apposition). Reproduced, with permission, from De Troyer A, Loring SH. Actions of the respiratory muscles. In: Roussos C, editor. The Thorax (2nd ed), Vol. 85. New York: Marcel Dekker, 1995, pp. 535‐563).



Figure 2.

Respiratory displacements of the rib cage. (A) diagram of a typical thoracic vertebra and a pair of ribs (viewed from above). Each rib articulates with both the body and the transverse process of the vertebra (closed circles) and is bound to it by strong ligaments (right). The motion of the rib, therefore, occurs primarily through a rotation around the axis defined by these articulations (solid line and double arrow‐head). (B) and (C) ventral and lateral views, respectively, of the rib at end expiration (solid lines) and end inspiration (dotted lines). When the rib becomes more horizontal in inspiration, the transverse (B) and the anteroposterior (C) diameter of the rib cage increase (small arrows), and the sternum is displaced ventrally (vertical line in C). Reproduced, with permission, from De Troyer A. Respiratory muscle function. In: Shoemaker WC, Ayres SM, Grenvik A, Holbrook PR, editors. Textbook of Critical Care. W.B. Saunders, 2000, pp. 1172‐1184).



Figure 3.

Mean ± SE changes in airway opening pressure (ΔPao) and abdominal pressure (ΔPab) obtained from six dogs during isolated, bilateral stimulation of the phrenic nerves at five different lung volumes from FRC (transrespiratory pressure = 0 cmH2O) to TLC (transrespiratory pressure = 30 cmH2O). All stimulations were performed while the endotracheal tube was occluded. The capacity of the diaphragm to generate pressure, in particular pleural pressure, decreases markedly with increasing lung volume. Reproduced, with permission, from ref. 49).



Figure 4.

Relationship between transdiaphragmatic pressure (Pdi) and diaphragm muscle length during isolated, supramaximal phrenic nerve stimulation at different lung volumes. The dashed line in the main panel is the aggregate relationship obtained for the costal and crural portions of the canine diaphragm in vivo by Road et al. 134, and the closed circles are the mean ± SE values obtained from six dogs (same animals as in Figure 3) during phrenic nerve stimulation at increasing lung volumes from FRC (top circle) to TLC (bottom circle). Muscle length was measured by computed tomography and is expressed as a percentage of muscle length during relaxation at FRC (LFRC). Note that the data point obtained at FRC is close to the length‐tension relationship of Road et al., but the data points obtained at high lung volumes lay well below the curve. Data in the inset are the mean values obtained before (closed circles) and after (open circle; bars, ± SE) bilateral pneumothorax in a subset of four animals. (Redrawn, with permission, from ref. 60).



Figure 5.

Graphical representation of the effect of inflation on the pressure developed by the diaphragm. The continuous lines are the Pdi‐length relationships for the maximally active and the passive diaphragm, and the dashed lines are the load lines describing the load imposed by the lung and chest wall on the diaphragm during isolated contraction at FRC and during isolated contraction at TLC. Pdi is expressed as a fraction of the maximal value, and muscle length is expressed as a fraction of optimal length (Lo). The pressure developed by the diaphragm during phrenic nerve stimulation at a given lung volume is given by the intersection (closed circle) of the load line with the maximally active Pdi‐length curve. Reproduced, with permission, from ref. 60).



Figure 6.

Graphical analysis of the pressure generated by the diaphragm in the presence of ascites. The continuous lines describing the Pdi‐length relationships for the maximally active and the passive diaphragm, and the dashed line describing the load line for the isolated diaphragm in the control condition are the same as those in Figure 5. The thin solid lines are the two load lines for the diaphragm in the presence of moderate and severe ascites. With moderate ascites, the relaxed diaphragm lengthens and the elastance of the abdomen increases, so that the load line is displaced upward and is more steep. As a result, the diaphragm during phrenic nerve stimulation shortens less and generates a larger pressure (closed triangle). With severe ascites, the load line is further displaced upward and still more steep, but the radius of diaphragm curvature during phrenic stimulation increases. Consequently, the active diaphragm is even longer, but the pressure generated (closed square) is smaller than anticipated on the basis of muscle length alone (open square).



Figure 7.

Contours of the diaphragm seen on anteroposterior radiographs in a dog during relaxation at FRC, during isolated tetanic stimulation of the right phrenic nerve (dashed line), and during combined stimulation of the left and right phrenic nerves. Stimulation frequency = 50 Hz. The two short bars on each contour correspond to the junctions of the muscle fibers with the central tendon and show the lateral shift of the tendon (and the mediastinum) during unilateral phrenic nerve stimulation. The surface area (volume) swept by the diaphragm during simultaneous contraction of the right and left hemidiaphragms is more than twice that swept when the right hemidiaphragm contracts in isolation.



Figure 8.

Diagram illustrating the actions of the intercostal muscles, as proposed by Hamberger 82. The two bars oriented obliquely in each panel represent two adjacent ribs. The external and internal (interosseous) intercostal muscles are depicted as single bundles, and the torques acting on the ribs during contraction of these muscles are represented by arrows. When the external intercostal contracts (A), the torque acting on the lower rib is greater than that acting on the upper rib; the opposite is true when the internal intercostal contracts (B). Reproduced, with permission, from ref. 45).



Figure 9.

Maximal respiratory effects of the canine external (A) and internal interosseous (B) intercostal muscles in the dorsal third, middle third, and ventral third of the even‐numbered interspaces (both sides of the sternum). The respiratory effects of the medial portion of the parasternal intercostals in interspaces 2, 4, 6, and 8 are also shown. Reproduced with permission from ref. 45).



Figure 10.

Effects of rib curvature on the net moment exerted by an intercostal muscle. (A) plan form of a typical rib in the dog and its axis of rotation (bold vector). At point a, the distances between the points of attachment of an intercostal muscle on the lower and upper ribs and the axes of rotation are different, and the muscle exerts a net moment on the ribs. At point b, however, the distances between the points of attachment of an intercostal muscle on the lower and upper ribs and the axes of rotation of the ribs are equal, and the muscle exerts no net moment. Thus the net moment exerted by the muscle depends on the angular position (θ) around the rib, as shown in (B). The external intercostal muscle (continuous line) has the greatest inspiratory moment in the dorsal portion of the rib cage (θ between 15 and 60°); this inspiratory moment then decreases as one moves around the rib cage (θ between 60 and 120°) and is reversed into an expiratory moment in the vicinity of the sternum (θ > 120°). The internal intercostal muscle (dashed line in B) shows a similar gradient in expiratory moment. Reproduced, with permission, from ref. 45).



Figure 11.

Effect on the lung of external loading of individual rib pairs in the cranial direction. Data are the mean ± SE values of the changes in airway opening pressure (ΔPao) per unit force (F) on the ribs obtained from seven animals. At FRC (closed circles), ΔPao /F increases from the second to the fifth rib pair and then decreases continuously to the eleventh rib pair. ΔPao /F for ribs 2 to 8, however, decreases markedly when lung volume is passively increased from FRC to 10 cmH2O (open circles) and 20 cmH2O (open triangles) transrespiratory pressure. Reproduced, with permission, from ref. 46.



Figure 12.

Patterns of rib displacement produced by the external and parasternal intercostals in the dog. In the animal in (A), the parasternal intercostals in interspaces 1 to 8 were denervated on both sides of the sternum; in the animal in (B), the parasternal intercostals were intact but the external intercostals in interspaces 1 to 8 were excised. Both animals had complete diaphragmatic paralysis. The dashed line in each panel is the trajectory of the ribs during passive inflation (relaxation), and the solid line with the arrowhead corresponds to a spontaneous inspiration. Reproduced, with permission, from ref. 58.



Figure 13.

Maximal inspiratory effects of the parasternal intercostal and external intercostal muscles in the even‐numbered interspaces in dogs (A) and in humans (B). Redrawn from ref 45, with permission.



Figure 14.

Effects of inflation on the pressure‐generating ability of the inspiratory intercostals. The closed circles are the mean ± SE values of ΔPao obtained from 19 dogs during isolated, tetanic stimulation of the inspiratory (and expiratory) intercostals at different lung volumes, as reported by DiMarco et al. 61. The open circles are the mean ± SE values of ΔPao obtained from 9 dogs during spontaneous contraction of the parasternal intercostals alone 102. Similar to the diaphragm, the pressure‐generating ability of the inspiratory intercostals decreases with increasing lung volume. Reproduced with permission from ref. 60.



Figure 15.

Dorsal view of the spine and one rib in its position at FRC and its position at 20 cmH2O transrespiratory pressure. Because the rib at FRC is slanted caudally, it moves both cranially (Xr) and outward (Yr) during cranial loading. However, at 20 cmH2O transrespiratory pressure, the rib is almost horizontal. Therefore, loading the rib causes a cranial displacement with little or no outward displacement. Reproduced with permission from ref. 46.



Figure 16.

Pattern of rib cage motion during mechanical ventilation (left) and during spontaneous breathing (right) in a quadriplegic subject with a traumatic transection of the upper cervical cord (C1). Each panel shows, from top to bottom, the respiratory changes in anteroposterior (AP) diameter of the lower rib cage, the changes in AP diameter of the upper rib cage, the changes in transverse diameter of the lower rib cage, and the changes in xiphi‐pubic distance. Upward deflections correspond to an increase in diameter or an increase in xiphi‐pubic distance (i.e., a cranial displacement of the sternum); I indicates the duration of inspiration. All rib cage diameters and the xiphi‐pubic distance increase in phase during mechanical inflation. When the sternomastoids contract forcefully during spontaneous inspiration, however, the xiphi‐pubic distance and the upper rib cage AP diameter increase proportionately more than the lower rib cage AP diameter, and the lower rib cage transverse diameter then decreases. Reproduced, with permission, from De Troyer A. Mechanics of the chest wall muscles. In: Miller AD, Bianchi AL, Bishop B, editors. Neural control of the respiratory muscles, CRC Press, Inc., 1996, pp. 59–73.

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André De Troyer, Aladin M. Boriek. Mechanics of the Respiratory Muscles. Compr Physiol 2011, 1: 1273-1300. doi: 10.1002/cphy.c100009