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1 Laboratory of Cardiorespiratory Physiology, Brussels School of Medicine, 1070 Brussels, Belgium2 Chest Service, Erasme University Hospital, 1070 Brussels, Belgium3 Intensive Care Unit, Saint-Pierre University Hospital, 1000 Brussels, Belgium
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Abstract |
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Pao) were measured in anaesthetized, pancuronium-treated, supine dogs while loads were applied in the cranial direction to individual rib pairs at functional residual capacity (FRC) and after passive inflation to 10 and 20 cmH2O transrespiratory pressure. In agreement with the hypothesis, inflation caused an increase in Pao for ribs 9 and 10. The most prominent alteration, however, was a marked decrease in Pao for ribs 2–8; at 20 cmH2O, Pao for these ribs was only 30% of the value at FRC. Additional measurements indicated that this decrease in Pao results partly from the increase in diaphragmatic compliance but mostly from the reduction in outward rib displacement. This alteration in the pattern of rib motion should add to the decrease in muscle length to reduce the lung expanding action of the external intercostal muscles at high lung volumes.
(Received 21 October 2003;
accepted after revision 15 December 2003;
first published online 23 December 2003)
Corresponding author A. De Troyer: Chest Service, Erasme University Hospital, Route de Lennik, 808, 1070 Brussels, Belgium. Email: a_detroyer{at}yahoo.fr
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Introduction |
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To assess the mechanism of this rostrocaudal gradient, we recently investigated the coupling between the different ribs and the lung by applying external loads to individual rib pairs in supine animals (De Troyer & Wilson, 2002). The rib displacement induced by a given load increased gradually with increasing rib number. However, the change in airway opening pressure (Pao) increased from the second to the fifth rib pair and then decreased markedly from the fifth to the eleventh rib pair. It was concluded therefore that the coupling between the ribs and the lung does vary from the top to the base of the rib cage, and it was further concluded that this coupling is indeed a primary determinant of the actions of intercostal muscles on the lung. Specifically, the coupling confers to both the external and the internal intercostal muscles an inspiratory action on the lung in the rostral interspaces and an expiratory action in the caudal interspaces.
The mechanism of the non-uniform coupling between the ribs and the lung is uncertain, but the speculation was offered that the effect of a particular rib on the lung is directly related to the area of the lung subtended by the rib (De Troyer & Wilson, 2002). In the dog, the radii of the ribs in the rostral half of the rib cage increase gradually with increasing rib number (Margulies et al. 1989). In this half of the rib cage, therefore, the area of the lung subtended by a particular rib should be greater than that subtended by the rib above, so the fall in Pao produced by a cranial displacement of that rib would also be greater. On the other hand, the ribs in the caudal half of the rib cage are in part apposed through the diaphragm to the abdomen, rather than the lung (Mead, 1979). Consequently, a cranial displacement of these ribs should primarily result in an expansion of the ventral abdominal wall and a fall in abdominal pressure, and the fall in Pao would be only secondary, due to the (passive) caudal displacement of the diaphragm (De Troyer & Wilson, 2002). The fall in Pao produced by a given cranial displacement of the most caudal ribs, therefore, would be smaller than the fall in abdominal pressure and smaller than the fall in Pao produced by the same cranial displacement of more cranial ribs.
In the present studies, we have tested these ideas by assessing the changes in both Pao and abdominal pressure during rib loading and by evaluating the effect of lung volume on the rib–lung coupling. Thus, the zone of apposition of the diaphragm to the rib cage decreases when lung volume is passively increased above functional residual capacity (Mead, 1979). With inflation, therefore, the area of the lung subtended by the caudal ribs should increase, so it would be expected that the coupling between these ribs and the lung would be improved.
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Methods |
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Fifteen minutes after instrumentation, the animal was injected with a neuromuscular blocking agent (2 mg pancuronium I.V.) and ventilated mechanically. After calibration of the displacement transducer, the ventilation was stopped and the chest wall was allowed to relax to equilibrium. The endotracheal tube was occluded, and 200 g lead balls were placed in both baskets attached to the second rib so that the load in each basket was increased by 0.2 kg increments from 0.2 to 0.6 kg. Two runs of loading were performed, after which a large syringe was connected to the endotracheal tube and the animal was inflated to a lung volume corresponding to a transrespiratory pressure of 10 cmH2O. Two runs of rib loading were also performed at this volume. The animal was finally inflated to a transrespiratory pressure of 20 cmH2O, and two runs of loading were also performed. The hookbasket system and the displacement transducer were then transferred to the third rib pair, and two runs of loading were obtained at 0, 10 and 20 cmH2O transrespiratory pressure. The procedure was repeated for every individual rib pair down to the eleventh pair.
These measurements indicated that the coupling between the ribs and the lung is indeed markedly altered by inflation (see Results). After the initial procedure was completed, two additional protocols were therefore followed.
Blood pressure and heart rate were monitored during the course of the experiments and no changes occurred. Also, the pupils in each animal remained constricted and unresponsive to light, thus indicating a deep level of anaesthesia. At the conclusion of the measurements, the animals were given an overdose (30–40 mg kg-1I.V.) of anaesthetic.
Data analysis
For each rib pair at each lung volume in each individual animal, the axial rib displacements (Xr) and the changes in Pao induced by each load (force, F) were averaged over the two runs. The relationships thus obtained between Xr and F and between Pao and F were then calculated by using linear regression techniques (coefficient of correlation, r between 0.925 and 0.999), and the slopes of these relationships (Xr/F and Pao/F) were averaged over the animal group. The changes in Pab and the lateral rib displacements (Yr) observed during rib loading were analysed similarly.
The changes in Pab and Ppl during passive inflation in each animal were also averaged over the two trials, and the alterations in (passive) diaphragmatic tension were evaluated by calculating the changes in transdiaphragmatic pressure (Pdi) along the lines suggested by Agostoni & Rahn (1960). Thus, at each level of inflation, the change in Ppl was subtracted from the change in Pab(Pdi=Pab-Ppl), and the Pdi thus obtained was adjusted to yield a value of 0 cmH2O at 1.0 litre above FRC. As for the data obtained during rib loading, the changes in Pab and Pdi during passive inflation were averaged over the animal group.
All data are presented as means ±S.E.M. Comparisons between the slopes for the different rib pairs and between the slopes obtained for a given rib pair at the three different lung volumes were made by analysis of variance (ANOVA) with repeated measures, and multiple comparison testing of the mean values was performed, when appropriate, using Student–Newman–Keuls tests. The criterion for statistical significance was taken as P < 0.05.
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Results |
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Pao and F are summarized in Fig. 2. In agreement with our previous observation (De Troyer & Wilson, 2002), Pao/F at FRC increased gradually from the second to the fifth rib pair and then declined from the fifth to the eleventh rib pair (Fig. 2A). This pattern was also observed during loading at 10 and 20 cmH2O transrespiratory pressure. With increasing lung volume, however, Pao/F for the second to seventh rib pairs decreased markedly (P < 0.001), such that at 10 and 20 cmH2O transrespiratory pressure, it amounted, respectively, to 55 ± 1 and 30 ± 1% of the FRC value (Fig. 2B). In contrast, Pao/F for the ninth rib pair was consistently greater at 10 cmH2O than at FRC (P < 0.05), and Pao/F for the tenth rib pair was greater at both 10 and 20 cmH2O than at FRC.
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Pab and F obtained during loading of the fourth and tenth rib pairs are compared with the slopes of the relationships between Pao and F in Fig. 3. When the tenth rib pair was loaded (Fig. 3, right), Pab/F was greater than Pao/F in every animal (P < 0.001), in particular at FRC. For the seven animals studied, the Pao/Pab ratio at FRC thus averaged 0.01 ± 0.12, and it increased (P= 0.03) to 0.22 ± 0.11 and 0.58 ± 0.27 at 10 and 20 cmH2O transrespiratory pressure, respectively. On the other hand, when the fourth rib pair was loaded (Fig. 3, left), Pab/F was consistently lower than Pao/F (P < 0.001) and the Pao/Pab ratio, which amounted to 3.12 ± 0.21 at FRC, decreased (P= 0.05) to 1.94 ± 0.26 at 20 cmH2O. Loading the fourth rib pair, however, also caused the tenth rib to move cranially at all lung volumes. Both at FRC and at 20 cmH2O, the slope of the relationship between the displacement of the tenth rib and F during the procedure was 22 ± 2% of the slope of the relationship obtained when the tenth rib pair itself was loaded, and the Pab/F corresponding to this displacement represented 27 ± 2% of the total Pab/F.
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Pdi was negative, thus indicating that tension in the diaphragm above FRC was reduced relative to FRC. In fact, although the rise in Pab was linearly related to lung volume, the relationship between Pdi and lung volume was curvilinear such that for a given volume increase, the reduction in Pdi decreased progressively as lung volume was greater.
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Discussion |
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Pao/Pab was much smaller than 1 during loading of the tenth rib pair at FRC (Fig. 3, right), whereas during loading of the fourth rib pair, Pao/Pab was greater than 1 (Fig. 3, left). Also, Pao/F for ribs 9–11 increased with inflation in every animal (Fig. 2). This increase, however, was moderate, and Pao/F for these ribs remained smaller than that for ribs 5–7 at all lung volumes, including at 20 cmH2O transrespiratory pressure. The most prominent effect of inflation, in fact, was a decrease in Pao/F for all the ribs situated cranial to the zone of apposition of the diaphragm to the rib cage.
The observation that Xr/F in our animals decreased as lung volume was increased above FRC (Fig. 1) confirms our previous finding that in the dog, cranial rib compliance at high lung volumes is lower than at FRC (De Troyer et al. 1985). All other things being equal, such a decrease in Xr/F should lead to a reduction in Pao/F for the ribs cranial to the zone of apposition. The decrease in Xr/F should also reduce the increase in Pao/F for the caudal ribs that the increase in the area of the lung subtended by these ribs would cause otherwise. However, the decrease in Xr/F with inflation was relatively small. For ribs 5–8, the change observed from FRC to 20 cmH2O transrespiratory pressure amounted to only 23% of the FRC value, whereas the corresponding reduction in Pao/F was 70% (Fig. 2B). Moreover, Xr/F for ribs 2–4 was unaffected by inflation, yet Pao/F for these ribs was similarly reduced by 70%. The volume-induced reduction in Pao/F must therefore result primarily from other mechanisms.
When forces are applied to a given rib pair in the cranial direction, the fall in airway opening (pleural) pressure elicits a cranial displacement of the passive diaphragm, and this displacement, in turn, causes a fall in abdominal pressure and reduces the fall in Pao. However, measurements of diaphragmatic muscle length (Sprung et al. 1990) and transdiaphragmatic pressure (Pengelly et al. 1971; Road et al. 1986; Hubmayr et al. 1990) have clearly established that in supine dogs and cats, the action of gravity on the abdominal visceral mass induces stretching and, with it, significant passive tension in the diaphragm at FRC. These measurements have also established that diaphragmatic compliance in such animals increases progressively as lung volume is passively increased above FRC, and indeed, during passive inflation, our animals demonstrated a gradual fall in transdiaphragmatic pressure with increasing lung volume (Fig. 4), and when the fourth rib pair was loaded, the Pao/Pab ratio decreased from FRC to 20 cmH2O transrespiratory pressure (Fig. 3, left). Because of this increase in diaphragmatic compliance, it would be expected that during rib loading at high lung volumes, a given Pao would lead to a greater cranial displacement of the diaphragm and therefore that the loss in Pao/F would also be greater.
The role played by this mechanism in determining the reduction in Pao/F at high lung volumes is examined in Fig. 7. The filled and open circles in this figure indicate, respectively, the changes in Pao and Pab measured during loading of the fourth rib pair at different lung volumes and previously shown in Fig. 3 (left). If diaphragmatic compliance did not increase with increasing lung volume but instead remained unchanged, then a given fall in Pao would induce at all lung volumes the same fall in Pab as it does at FRC, and the Pao/Pab ratio would be constant. Using the values of Pab measured during loading at the different lung volumes in our animals and the Pao/Pab ratio measured at FRC, one can therefore calculate the values of Pao/F that would be obtained in this condition. The results of these calculations are represented by the dashed line in Fig. 7. At the lung volume corresponding to 10 cmH2O transrespiratory pressure, the calculated Pao/F amounted to -2.6 cmH2O, whereas the measured value was -1.7 cmH2O. In other words, the increase in diaphragmatic compliance from FRC to 10 cmH2O transrespiratory pressure would yield a 25% reduction in Pao/F, i.e. it would account for about half of the total loss in Pao/F. Similarly, the greater diaphragmatic compliance at 20 cmH2O transrespiratory pressure would account for a 15% reduction in Pao/F, representing 20% of the total loss.
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Pao/F during rib loading but also in a greater fall in Pab. Consequently, to the extent that the calculated values of Pao/F were computed on the basis of the measured Pab values, they tend to overestimate the effect of the increase in diaphragmatic compliance. Second, the analysis in Fig. 7 rests on the assumption that loading of the fourth rib pair has no effect on Pab other than via the diaphragm. In fact, loading of these ribs also led to a cranial displacement of the most caudal ribs, and this displacement must have affected the abdominal wall and Pab in much the same way as it does when the caudal ribs themselves are loaded. This displacement, however, was small at all lung volumes and corresponded to a relatively small fraction of the total Pab measured during loading of the fourth rib pair, thus suggesting that it was not a key factor. Finally, the analysis in Fig. 7 also rests on the assumption that the compliance of the abdominal wall remains constant with increasing lung volume. The observation in our animals that the relationship between lung volume and Pab during passive inflation is linear (Fig. 4) supports this assumption; a linear volume–Pab relationship during passive inflation has also been reported in supine cats (Pengelly et al. 1971). Yet, because we measured lung, rather than abdominal volume, the possibility still exists that as in humans (Grimby et al. 1976; Hill et al. 1984), the abdominal wall in supine dogs would be stiffer at high lung volumes than at FRC. Such a change, however, would only impede the cranial displacement of the diaphragm at high lung volumes, and this would also reduce the loss in Pao/F. Thus, even though the losses in Pao/F attributed to the increase in diaphragmatic compliance in Fig. 7 are approximate, the conclusion can safely be drawn that this increase is not the main determinant of the volume-induced reduction in the rib–lung coupling. On the other hand, the ribs in the dog are slanted caudally at FRC and move primarily through a rotation around the axis defined by their vertebral articulations (Margulies et al. 1989). It would be expected therefore that as the ribs rotate cranially with inflation and become orientated more transversally relative to the sagittal midplane, a given cranial rib displacement would be associated with a smaller outward displacement, as shown in Fig. 8. Furthermore, in a previous study of the patterns of rib motion produced by the actions of the canine parasternal and external intercostal muscles, it was shown that a given outward displacement of the ribs during breathing is much more effective in increasing lung volume than the same rib displacement in the cranial direction (De Troyer & Wilson, 2000). Consequently, the speculation was also raised that a decrease in outward rib displacement at high lung volumes would play a major role in causing the observed reduction in rib–lung coupling.
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Pao produced by an axial rib displacement of 1 mm is denoted a, the relationship between rib displacement and Pao/F during loading at a given lung volume can therefore be expressed, to a good approximation, by the following equation:
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Pao/F at 10 cmH2O transrespiratory pressure would amount to 75% of the FRC value. In other words, at this lung volume, the reduction in Pao/F due to the alteration in rib displacement alone (i.e. independent of any concomitant increase in diaphragmatic compliance) would be 25% of the FRC value. At 20 cmH2O transrespiratory pressure, the isolated alteration in rib displacement would also yield a 47% reduction in Pao/F, and these two values are close to those predicted on the basis of the measured changes in Pab/F. Indeed, the analysis developed in Fig. 7 suggested that the reduction in Pao/F unrelated to diaphragmatic compliance was 
26% of the FRC value at 10 cmH2O and 55% at 20 cmH2O. Overall the measurements of Pab and rib displacement, while based on independent techniques, thus lead to the conclusion that the decrease in rib–lung coupling at high lung volumes results partly from the increase in diaphragmatic compliance but mostly from the reduction in outward rib displacement. As a corollary, to the extent that the bucket-handle rotation of the human ribs during passive inflation (Wilson et al. 2001) is similar in magnitude to that observed in the dog (Margulies et al. 1989), one would further predict that the coupling between the ribs and the lung in humans would also decrease markedly with increasing lung volume. When the ribs in our animals were loaded, their cranial displacement was consistently greater than their outward displacement relative to the relaxation curve (Fig. 5). The pattern of rib motion induced by loading thus closely reproduced the pattern of rib motion caused by an isolated contraction of the external intercostal muscles (De Troyer & Wilson, 2000), and it is well known that the pressure-generating ability of these muscles decreases markedly as lung volume is increased above FRC (Di Marco et al. 1990). This decrease has conventionally been attributed to the length–tension characteristics of the muscles, and indeed the external intercostals, particularly those in the rostral interspaces, shorten gradually as lung volume is increased (Di Marco et al. 1992; De Troyer et al. 1999). The current findings, however, have established that the pattern of rib motion would result in a marked decrease in the pressure-generating ability of these muscles even though the length of the muscles was kept constant and the force generated by them was preserved.
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References |
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De Troyer A & Kelly S (1982). Chest wall mechanics in dogs with acute diaphragm paralysis. J Appl Physiol 53, 373–379.
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Acknowledgements |
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This article has been cited by other articles:
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  A. De Troyer and D. Leduc Effects of single-lung inflation on inspiratory muscle function in dogs J. Physiol., October 1, 2006; 576(1): 269 - 277. [Abstract] [Full Text] [PDF]
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 A. De Troyer and D. Leduc Effect of diaphragmatic contraction on the action of the canine parasternal intercostals J Appl Physiol, July 1, 2006; 101(1): 169 - 175. [Abstract] [Full Text] [PDF]
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D. Leduc and A. D. Troyer The effect of lung inflation on the inspiratory action of the canine parasternal intercostals J Appl Physiol, March 1, 2006; 100(3): 858 - 863. [Abstract] [Full Text] [PDF]
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 A. De Troyer, P. A. Kirkwood, and T. A. Wilson Respiratory Action of the Intercostal Muscles Physiol Rev, April 1, 2005; 85(2): 717 - 756. [Abstract] [Full Text] [PDF]
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), and 20 cmH2O transrespiratory pressure (
).
