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Laboratory of Cardiorespiratory Physiology, Brussels School of Medicine, Brussels, and Chest Service, Erasme University Hospital, Brussels; and Intensive Care Unit, Saint-Pierre University Hospital, Brussels, Belgium
Submitted 21 November 2005 ; accepted in final form 2 March 2006
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ABSTRACT |
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Pao) produced by a given force on the ribs was invariably greater during phrenic nerve stimulation than with the diaphragm relaxed. The cranial rib displacement (Xr), however, was 40–50% smaller, thus indicating that the increase in Pao was exclusively the result of the increase in diaphragmatic elastance. In the second experiment, the parasternal intercostal muscle in the fourth interspace was selectively activated, and the effects of diaphragmatic contraction on the Pao and Xr caused by parasternal activation were compared with those observed during the application of external loads on the ribs. Stimulating the phrenic nerves increased the Pao and reduced the Xr produced by the parasternal intercostal, and the magnitudes of the changes were identical to those observed during external rib loading. It is concluded, therefore, that the diaphragm has no significant synergistic or antagonistic effect on the force developed by the parasternal intercostals during breathing. This lack of effect is probably related to the constraint imposed on intercostal muscle length by the ribs and sternum. respiratory muscles; muscle interaction; chest wall mechanics; rib-lung coupling
Previous studies of the mechanical interactions among the intercostal muscles have suggested that the insertions of the muscles on the ribs, the costal cartilages, and the sternum impose significant constraint on their length and, with it, on their force-generating ability. Specifically, in the dog with the airway occluded at functional residual capacity (FRC), the change in airway opening pressure (Pao) produced by the simultaneous, bilateral contraction of the parasternal intercostals or external intercostals in two interspaces is, within 10%, equal to the sum of the Pao values produced by bilateral contraction of the muscles in each individual interspace (27). The Pao produced by the simultaneous contraction of the parasternal or external intercostals in one or two interspaces on the left and right sides of the sternum is also nearly equal to the sum of the Pao values produced by separate left and right contraction (2). On the other hand, when the phrenic nerves in dogs (8) and in humans (1) are selectively stimulated, the Pao obtained during bilateral stimulation is clearly greater than the sum of the Pao values obtained during separate left and right stimulation. Thus, apparently, in contrast to the diaphragm, the intercostal muscles have small enough changes in length and remain near enough to their optimum force-producing lengths that the synergistic or antagonistic interactions between them are negligible. On this basis, therefore, it would be reasonable to speculate that the force-generating ability of the intercostal muscles remains essentially unchanged during contraction of the diaphragm.
In the present studies, the hypothesis was thus tested that the diaphragm causes little or no alteration in the force-generating ability of the canine parasternal intercostals. The parasternal intercostals were selected for the study because they are more easily accessible than the external intercostals and also because, in the dog, they are the main determinant of the inspiratory elevation of the ribs (5). The force generated by the parasternal intercostals during breathing, however, cannot be measured directly. Furthermore, because an isolated contraction of these muscles causes a (passive) cranial displacement of the diaphragm, which corresponds to a pressure dissipation, it would be expected that a particular force generated by the parasternal intercostals in the presence of diaphragmatic activity would lead to a greater fall in Ppl than if the same parasternal force were generated with the diaphragm relaxed. If so, it would also be difficult to estimate the force developed by these muscles on the basis of Ppl measurements alone. To overcome this difficulty, we combined two procedures. First, we applied external forces to the different ribs and determined the effect of diaphragmatic contraction on the lung expansion produced by such forces. Next, we assessed the effect of diaphragmatic contraction on the lung expansion produced by selective activation of the parasternal intercostals. By comparing this effect with that measured during the application of external forces on the ribs, we could therefore evaluate the potential effect of diaphragmatic contraction on the force generated by the parasternal intercostals.
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METHODS |
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Experiment 1. Six animals were studied first to assess the effect of diaphragmatic contraction on the coupling between the ribs and the lung. The method used to determine this coupling has been previously described (13, 16). Thus hooks were screwed into the fourth right and left bony ribs, 1 cm lateral to the costochondral junctions. A long inextensible thread was attached to each hook and led cranially, parallel to the longitudinal body axis of the animal, over a pulley placed at the head of the table, and it was connected to a small basket in which weights could be placed later. An additional hook was screwed into the fourth right rib in the midaxillary line and connected to a linear displacement transducer (Schaevitz Engineering, Pennsauken, NJ) to measure the craniocaudal (axial) rib displacement (11). After the animal was made apneic by mechanical hyperventilation, the endotracheal tube was occluded at resting end expiration (FRC), and 200-g lead balls were placed in both baskets attached to the fourth rib so that the load in each basket was increased by 0.2-kg increments from 0.2 to 0.8 kg. Two runs of loading were performed. The animal was then reconnected to the ventilator and hyperventilated, and square pulses of 0.1-ms duration and supramaximal voltage were applied at a frequency of 20 impulses/s to the left and right C5 and C6 phrenic nerve roots. The stimulation was maintained for 4–8 s, at which time the endotracheal tube was occluded and loads were applied again to the fourth rib pair. This time interval allowed the respiratory system to reach equilibrium (i.e., the diaphragm after 4–8 s caused no further change in Pao), such that the effects of the loads on the rib and Pao could be accurately determined. To reduce the total number of phrenic nerve stimulations and maintain diaphragmatic contractility constant throughout the experiment, only two loads, namely 0.4 and 0.8 kg, were applied in this condition. As during control, however, two trials were obtained with each load.
After completion of these measurements, the two hooks and baskets and the displacement transducer were transferred to the fifth rib pair, and two runs of loading were performed, first with the diaphragm relaxed and then during tetanic stimulation of the C5–C6 phrenic nerves. The procedure was subsequently repeated for each individual rib pair down to the 10th pair. For the fifth rib pair, however, an additional thread was attached to the hook in the midaxillary line and led laterally, perpendicular to the sagittal midplane, to measure both the lateral and the axial rib displacement (11).
Experiment 2. Six animals were studied next to assess the effect of diaphragmatic contraction on the force generated by the parasternal intercostals. Two successive procedures were used in each animal. The first procedure was similar to that used in experiment 1 and involved applying cranially oriented loads to the fifth rib pair, first with the diaphragm relaxed and then during tetanic stimulation of the phrenic nerves. Next the parasternal intercostal muscle in the fourth interspace was selectively activated by using a pair of stimulating electrodes implanted in the muscle on either side of the sternum. These electrodes were silver hooks insulated with polyethylene tubing except for their terminal 8 mm, and their implantation was made superficially along muscle bundles situated in the vicinity of the sternum, i.e., in the area of the parasternal intercostal muscle with the greatest inspiratory mechanical advantage (14). The internal intercostal nerve in the fourth interspace was also sectioned at the chondrocostal junction so as to avoid both antidromic stimulation of the internal interosseous intercostal muscle in the fourth interspace and stimulation, through spindle afferents, of intercostal muscles in contiguous segments (18, 24).
The animal was allowed to recover for 15–20 min after instrumentation, after which it was made apneic by mechanical hyperventilation. Square pulses of 0.2-ms duration and 20-Hz frequency were then delivered at intervals to the parasternal intercostal muscle. The stimulus intensity was increased by increasing the voltage of stimulation. At least four voltages, usually between 6 and 15 V, were used in each animal, and for each voltage, two trials of stimulation with the diaphragm relaxed alternating with two trials of stimulation superimposed on tetanic phrenic nerve stimulation were performed. The sequence of events in such trials was the same as that used for external rib loading. That is, with the animal apneic, stimulation was delivered to the phrenic nerves, and when equilibrium was achieved, the endotracheal tube was occluded and the parasternal intercostal was stimulated.
Experiment 3. Stimulating the phrenic nerves induced a marked caudal displacement of the ribs (see RESULTS). Consequently, the parasternal intercostal muscles before contraction were longer during phrenic nerve stimulation than with the diaphragm relaxed, and this difference in length could alter the force-generating ability of the muscles independent of any effect of diaphragmatic contraction. Six animals were studied to overcome the potential influence of this confounding factor. The procedure initially was identical to that described in experiment 2 and involved cranial loading of the fifth rib pair with the diaphragm relaxed and during tetanic stimulation of the C5–C6 phrenic nerve roots. The parasternal intercostal muscle in the fourth interspace was also activated with the diaphragm relaxed. At this stage, however, a nonelastic strap was placed around the abdomen from the pubis to the rib cage margin to increase abdominal elastance and to reduce the caudal rib displacement during phrenic nerve stimulation. External loading of the fifth rib pair and activation of the parasternal intercostal during phrenic stimulation were then repeated.
The animals were maintained at a constant, rather deep level of anesthesia throughout the study. They had no corneal reflex, no limb movement, and no changes in blood pressure and heart rate, including during phrenic nerve stimulation. At the conclusion of the measurements, the animal was given an overdose of anesthetic (30–40 mg/kg iv).
Data analysis.
For each rib in each animal of experiment 1, the changes in Pao (Pao) and the axial rib diplacements (Xr) induced by each load [force (F)] with the diaphragm relaxed and during phrenic nerve stimulation were averaged over the two runs. The relationships thus obtained between Pao and F and between Xr and F were then calculated by using linear regression techniques (coefficient of correlation between 0.974 and 0.999), and the slopes of these relationships (Pao/F and Xr/F) were averaged over the animal group. The lateral rib displacements (Yr) measured during loading of the fifth rib pair were analyzed similarly. By convention, Xr and Yr were assigned a positive sign when displacement was cranial and outward, respectively.
For each individual animal of experiments 2 and 3, the Pao and Xr induced by each parasternal intercostal stimulation (i.e., each stimulation intensity) with the diaphragm relaxed were also averaged over the two runs, and these values were then multiplied by the ratios between the slopes of the relationships (Pao/F and Xr/F) obtained during loading of the fifth rib pair with phrenic nerve stimulation and the slopes obtained during rib loading with the diaphragm relaxed. These computed Pao and Xr values thus correspond to the values that parasternal contraction would yield when superimposed on phrenic nerve stimulation if the force generated by the parasternal intercostal were unaltered by diaphragmatic contraction. These values, which will be referred to here as the "predicted" values, were then compared with the Pao and Xr values measured when parasternal stimulation was performed during phrenic nerve stimulation. The measured and predicted values of Pao and Xr obtained for the different stimulation intensities were then averaged in each animal, and they were finally averaged over the animal group.
All data are presented as means ± SE. Comparisons between the slopes Pao/F and Xr/F obtained for the different rib pairs during loading with and without phrenic nerve stimulation (experiment 1) were made by ANOVA with repeated measures, and multiple comparison testing of the mean values was performed, when appropriate, using Student-Newman-Keuls tests. Comparisons between the values of Pao and Xr obtained during parasternal intercostal contraction superimposed on phrenic nerve stimulation and the values obtained during parasternal contraction with the diaphragm relaxed (experiments 2 and 3) were made by using paired t-tests, as were the comparisons between the measured and predicted values. Statistical assessment of the effects of abdominal strapping on change in Pab (Pab) and rib axial displacement during phrenic nerve stimulation (experiment 3) was also made by using paired t-tests. The criterion for statistical significance was taken as P < 0.05.
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RESULTS |
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Pao and F and between Xr and F obtained for all the ribs during loading with the diaphragm relaxed (control) and during loading in the presence of phrenic nerve stimulation are shown in Fig. 1. In agreement with our laboratory's previous observations (13, 16), Pao/F during control increased from the 4th to the 6th rib pair and then decreased from the 6th to the 10th rib pair (Fig. 1A), whereas Xr/F increased continuously (P < 0.001) from the 5th to the 10th rib (Fig. 1B). With phrenic nerve stimulation, Pab in the six animals increased by 6.8 ± 0.4 cmH2O and the ribs moved caudally relative to their resting, end-expiratory position; the magnitude of this displacement varied with rib number and ranged between 5.27 ± 0.50 mm (rib 4) and 8.00 ± 0.72 mm (rib 9). When the ribs were loaded in this condition, however, Pao/F was consistently greater than during control (P < 0.001), whereas Xr/F was consistently smaller (P < 0.001). As shown in Fig. 2, the loss in Xr/F, when expressed as a percentage of the control value, was relatively uniform across the rib cage. In contrast, the increase in Pao/F was similar for ribs 4–6 but then increased markedly from rib 7 to rib 10 (P < 0.001).
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Pao and Xr obtained in a representative animal during bilateral contraction of the fourth parasternal intercostal muscle in the control condition and during the same parasternal intercostal contraction superimposed on phrenic nerve stimulation are shown in Fig. 4A, and the values of Pao and Xr obtained for all stimulation intensities in the same animal are shown in Fig. 4, B and C, respectively. Stimulating the parasternal intercostal in the control condition (
) produced a cranial displacement of the fifth rib and a fall in Pao, and these effects increased in magnitude as the intensity of stimulation was increased. A similar pattern was observed when stimulation of the parasternal intercostal was superimposed on phrenic nerve stimulation (
). For any given stimulation intensity, however, Pao was greater when parasternal contraction was superimposed on phrenic nerve stimulation than it was during control. In contrast, Xr was consistently smaller. In agreement with experiment 1, however, when external forces were applied to the fifth rib pair in this particular animal, Pao/F increased from –1.80 cmH2O/kg during control to –2.70 cmH2O/kg during phrenic nerve stimulation, and Xr/F decreased from +8.70 to +6.00 mm/kg. If the force generated by the parasternal intercostal muscle were unaltered by phrenic nerve stimulation, one would therefore predict that the Pao produced by this muscle would increase by 50% with phrenic stimulation, whereas Xr would decrease by 46%. The predicted values of Pao and Xr are represented by the plus signs in Fig. 4, B and C. As can be seen, the measured values agreed well with the predicted values. When the data obtained for all stimulation intensities were averaged, the measured and predicted values of Pao in this animal thus amounted to –2.14 and –2.23 cmH2O, respectively; the measured and predicted values for Xr were +1.30 and +1.17 mm.
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Pao during parasternal contraction in the control condition was –2.45 ± 0.28 cmH2O, and Xr was +4.63 ± 0.76 mm. When the phrenic nerves were stimulated, causing a rise in Pab of +9.2 ± 0.5 cmH2O and a caudal rib displacement of 5.83 ± 0.39 mm, Pao during parasternal contraction was increased to –3.22 ± 0.29 cmH2O (P < 0.001), and Xr was reduced to +2.40 ± 0.31 mm (P < 0.01). These two values, however, were not different from the predicted values (Pao: –3.17 ± 0.26 cmH2O; Xr = +2.63 ± 0.37 mm).
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Pab induced by phrenic stimulation in the six animals increased from +8.6 ± 0.7 to +25.3 ± 3.0 cmH2O (P < 0.01), and the caudal displacement of the fifth rib decreased from 5.07 ± 0.65 to 0.58 ± 0.36 mm (P < 0.001). Strapping the abdomen, however, did not affect Xr/F or Pao/F during rib loading in the presence of phrenic stimulation. In addition, the effects of phrenic stimulation on the alterations induced by contraction of the parasternal intercostal were similar to those observed in experiment 2 (i.e., without abdominal strapping). Thus the Pao produced by contraction of the fourth parasternal intercostal increased from –2.44 ± 0.25 cmH2O during control to –3.34 ± 0.31 cm H2O during phrenic stimulation (P < 0.01), Xr was reduced from +4.31 ± 0.52 to + 2.33 ± 0.31 mm (P < 0.01), and the measured values of Pao and Xr, here too, were nearly the same as the predicted values (Fig. 5). |
DISCUSSION |
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Pao during phrenic stimulation would have been larger had the cranial rib displacement been maintained. Furthermore, previous studies have shown that in the dog, rib displacement in the outward direction is about four times more effective in causing lung expansion than rib displacement in the cranial direction (13, 15). Consequently, an increase in the ratio of the outward rib displacement over the Xr during phrenic stimulation could have accounted for the increase in Pao. Rib loading during phrenic stimulation, however, drove the ribs along the same trajectory as it did with the diaphragm relaxed (Fig. 3). The increase in Pao must, therefore, be primarily related to the increase in diaphragmatic elastance.
Although the increase in Pao during phrenic stimulation was seen for all the ribs, it is noteworthy that this increase was particularly prominent for the most caudal ribs (Fig. 2A). This result, in fact, supports our laboratory's previous suggestion that the effect of a particular rib on the lung is directly related to the area of the lung subtended by the rib (16). Thus, at FRC, whereas the ribs in the cranial half of the rib cage are apposed to the lung, the most caudal ribs are apposed to the abdomen through the diaphragm. Therefore, with the diaphragm relaxed, a cranially oriented force on these ribs results primarily in an expansion of the abdominal wall and a fall in Pab, and the fall in Pao is small, due to the small passive caudal displacement of the diaphragm. On the other hand, when the phrenic nerves were stimulated, there was a marked caudal displacement of the diaphragm, as shown by the large rise in Pab. Previous radiographic measurements of diaphragmatic configuration in dogs have shown that with such phrenic nerve stimulation, the zone of apposition of the diaphragm to the rib cage is actually abolished (7, 8). In this condition, therefore, the most caudal ribs are also largely apposed to the lung, and external forces applied to them in the cranial direction can also generate significant falls in Pao.
On the basis of these findings, it was expected that unless the force generated by the parasternal intercostals was markedly reduced by diaphragmatic contraction, the Pao produced by a given parasternal activation would be greater during phrenic nerve stimulation than with the diaphragm relaxed. In agreement with this prediction, all animals in experiment 2 showed indeed a greater Pao when contraction of the parasternal intercostal was superimposed on phrenic nerve stimulation. The second important result of this study, however, is the observation that this increase in Pao was similar in magnitude to that observed when external loads were applied to the ribs (Figs. 4 and 5). The adverse effect of phrenic nerve stimulation on the Xr produced by the parasternal intercostal was also quantitatively similar to that observed during the application of external loads, thus indicating that in this experimental condition, the beneficial effect of diaphragmatic contraction on the lung expanding action of the parasternal intercostals was entirely related to the increase in diaphragmatic elastance. In other words, the force generated by the parasternal intercostals appeared to be unaffected by contraction of the diaphragm.
A possible complication to this experiment is that contraction of the parasternal intercostal was initiated well after the diaphragm was fully activated. As previously pointed out for the diaphragm (see the introduction), the force developed by a particular muscle during contraction is primarily determined by its length, and muscle length, in turn, is determined by the length-tension characteristics of the muscle and by the load imposed on the muscle (7). Therefore, there is no reason to believe that the late contraction of the parasternal intercostal would, by itself, alter the force generated by the muscle. However, the early, isolated stimulation of the phrenic nerves caused a marked caudal displacement of the ribs, thus implying that the parasternal intercostals before contraction were lengthened and displaced away from their in vitro optimum force-producing length (19). In addition, the rib cage in the dog becomes less compliant when it contracts below its resting, end-expiratory volume (3, 8). Therefore, the rib cage during phrenic nerve stimulation was also stiffer than it was with the diaphragm relaxed, so it would be expected that a given force on the ribs would induce a smaller rib displacement. And indeed, during phrenic stimulation in experiment 2, the Xr produced both by external forces on the ribs and by activation of the parasternal intercostals was invariably decreased (Figs. 1B and 4C). Consequently, the shortening of the muscles during contraction was reduced, and this reduction, combined with the increase in muscle length before contraction, might have obscured any synergistic or antagonistic effect that the diaphragm may have otherwise on these muscles.
When the abdomen was bound with nonelastic straps and the ribs during phrenic stimulation were maintained near their FRC position (experiment 3), however, the effects of diaphragmatic contraction on Pao and Xr produced by the parasternal intercostals remained quantitatively similar to the effects of diaphragmatic contraction on the changes produced by external forces on the ribs (Fig. 5). The abdominal straps, however, did not alter the rib or the pressure response to such external forces, thus suggesting that they did not impact on the action of the parasternal intercostal muscle being studied. In agreement with our hypothesis, therefore, the conclusion can be drawn that diaphragmatic contraction does not significantly alter the force generated by the parasternal intercostals. Furthermore, to the extent that this lack of effect would be the result of the constraint imposed on the parasternal intercostals by the sternum and the costal cartilages, it would be expected that this conclusion would also apply to humans regardless of the difference in shape between the canine and the human rib cage.
The question remains, however, as to why the Xr associated with a particular activation of the parasternal intercostals was still reduced when phrenic stimulation was performed with the abdomen bound (experiment 3). Because the ribs in this condition were maintained near their FRC position, it was expected that rib cage elastance would be unaltered and, hence, that the Xr during parasternal contraction would be maintained. The mechanism for the persistent reduction in cranial rib displacement during phrenic stimulation with the abdomen bound cannot be defined at this stage, but it must be pointed out that the Xr and the fall in Pao (and in Ppl) are mutually related. To be sure, the cranial displacement of the ribs during contraction of the parasternal intercostals causes the fall in Ppl, but at the same time, the fall in pressure does oppose the Xr. Because the fall in Ppl generated by the parasternal intercostal was greater when the muscle contraction was superimposed on phrenic stimulation, the force opposing the cranial rib displacement should therefore be greater. Until the effectiveness of Ppl in opposing the displacement of the ribs is quantified, however, the role of this mechanism remains speculative.
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GRANTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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