Expiratory muscle contribution to tidal volume in head-up dogs

A change from the supine to the head-up posture in anesthetized dogs elicits increased phasic expiratory activation of the rib cage and abdominal expiratory muscles. However, when this postural change is produced over a 4- to 5-s period, there is an initial apnea during which all the muscles are silent. In the present studies, we have taken advantage of this initial silence to determine functional residual capacity (FRC) and measure the subsequent change in end-expiratory lung volume. Eight animals were studied, and in all of them end-expiratory lung volume in the head-up posture decreased relative to FRC [329 +/- 70 (SE) ml]. Because this decrease also represents the increase in lung volume as a result of expiratory muscle relaxation at the end of the expiratory pause, it can be used to determine the expiratory muscle contribution to tidal volume (VT). The average contribution was 62 +/- 6% VT. After denervation of the rib cage expiratory muscles, the reduction in end-expiratory lung volume still amounted to 273 +/- 84 ml (49 +/- 10% VT). Thus, in head-up dogs, about two-thirds of VT result from the action of the expiratory muscles, and most of it (83%) is due to the action of the abdominal rather than the rib cage expiratory muscles.     

Role of the diaphragm in chest wall mechanics.

We analyzed three different assumptions about diaphragm function that determine the thoracoabdominal interaction. In the simplest case, the diaphragm is assumed to be a completely flaccid membrane serving only to partition the thorax and the abdominal cavity. In the second case, it is assumed to have a finite tension but to maintain a relatively flat surface at the base of the rib cage (i.e., a negligible zone of apposition). In the general case, it is assumed that the diaphragm has finite tension and its position may vary (i.e., permitting a zone of apposition). These possible modes of behavior are incorporated into a mathematical model of ventilatory system mechanics that distinguishes the diaphragm, lung, abdomen, and rib cage. The significance of these modes is examined with respect to data from human experiments in which gas or liquid is introduced into the pleural or abdominal spaces, causing a volume change (Vep). We show that the Vep effect on the thoracic and abdominal volumes is sensitive to diaphragm mechanics and depends on the nature of the Vep: gastric distension (with water or air) or pneumothorax. Only the behavior of the general model is consistent with physiological observations, especially the distribution of Vep. Our general mathematical model can quantitatively predict this behavior.     

Acute effects of thixotropy conditioning of inspiratory muscles on end-expiratory chest wall and lung volumes in normal humans.

Thixotropy conditioning of inspiratory muscles consisting of maximal inspiratory effort performed at an inflated lung volume is followed by an increase in end-expiratory position of the rib cage in normal human subjects. When performed at a deflated lung volume, conditioning is followed by a reduction in end-expiratory position. The present study was performed to determine whether changes in end-expiratory chest wall and lung volumes occur after thixotropy conditioning. We first examined the acute effects of conditioning on chest wall volume during subsequent five-breath cycles using respiratory inductive plethysmography (n = 8). End-expiratory chest wall volume increased after conditioning at an inflated lung volume (P < 0.05), which was attained mainly by rib cage movements. Conditioning at a deflated lung volume was followed by reductions in end-expiratory chest wall volume, which was explained by rib cage and abdominal volume changes (P < 0.05). End-expiratory esophageal pressure decreased and increased after conditioning at inflated and deflated lung volumes, respectively (n = 3). These changes in end-expiratory volumes and esophageal pressure were greatest for the first breath after conditioning. We also found that an increase in spirometrically determined inspiratory capacity (n = 13) was maintained for 3 min after conditioning at a deflated lung volume, and a decrease for 1 min after conditioning at an inflated lung volume. Helium-dilution end-expiratory lung volume increased and decreased after conditioning at inflated and deflated lung volumes, respectively (both P < 0.05; n = 11). These results suggest that thixotropy conditioning changes end-expiratory volume of the chest wall and lung in normal human subjects.     

Dependence of diaphragmatic length on lung volume and thoracoabdominal configuration

Changes in lung volume can be partitioned into volume displacements of the rib cage and abdomen. Abdominal displacements are often used as estimates of diaphragmatic displacements and changes in lengthening of diaphragmatic muscle. We used X-rays, ultrasound, and linear measurements of thoracic and abdominal diameters to estimate relationships among lung volume, thoracoabdominal configuration and diaphragmatic length, and we found that diaphragmatic length was strongly dependent on rib cage as well as abdominal displacement. In three subjects, the diaphragm shortened 57-85% as much during a breath made without abdominal displacement as during a normal breath in which the abdominal wall moved outward with the rib cage. We conclude that changes in diaphragmatic length can be estimated from surface measurements without radiation and that the length of the diaphragm cannot be estimated from displacements of the abdominal wall alone.     

Vagal modulation of respiratory muscle activity in awake dogs during exercise and hypercapnia.

Using chronically instrumented awake tracheotomized dogs, we examined the contributions of vagal feedback to respiratory muscle activities, both electrical and mechanical, during normoxic hypercapnia (inspired CO2 fraction = 0.03, 0.04, 0.05, and 0.06) and during mild treadmill exercise (3, 4.3, and 6.4 km/h). Cooling exteriorized vagal loops eliminated both phasic and tonic mechanoreceptor input during either of these hyperpneas. At a given chemical or locomotor stimulus, vagal cooling caused a further increase in costal, crural, parasternal, and rib cage expiratory (triangularis sterni) muscles. No further change in abdominal expiratory muscle activity occurred secondary to vagal cooling during these hyperpneas. However, removal of mechanoreceptor input during hypercapnia was not associated with consistent changes in end-expiratory lung volume, as measured by the He-N2 rebreathe technique. We conclude that during these hyperpneas 1) vagal input is not essential for augmentation of expiratory muscle activity and 2) decrements in abdominal expiratory muscle activity may be offset by increments in rib cage expiratory muscle activity and contribute to the regulation of end-expiratory lung volume.     

Chest wall kinematics and respiratory muscle action in walking healthy humans.

We studied chest wall kinematics and respiratory muscle action in five untrained healthy men walking on a motor-driven treadmill at 2 and 4 miles/h with constant grade (0%). The chest wall volume (Vcw), assessed by using the ELITE system, was modeled as the sum of the volumes of the lung-apposed rib cage (Vrc,p), diaphragm-apposed rib cage (Vrc,a), and abdomen (Vab). Esophageal and gastric pressures were measured simultaneously. Velocity of shortening (V(di)) and power [Wdi = diaphragm pressure (Pdi) x V(di)] of the diaphragm were also calculated. During walking, the progressive increase in end-inspiratory Vcw (P < 0.05) resulted from an increase in end-inspiratory Vrc,p and Vrc,a (P < 0.01). The progressive decrease (P < 0.05) in end-expiratory Vcw was entirely due to the decrease in end-expiratory Vab (P < 0.01). The increase in Vrc,a was proportionally slightly greater than the increase in Vrc,p, consistent with minimal rib cage distortion (2.5 +/- 0.2% at 4 miles/h). The Vcw end-inspiratory increase and end-expiratory decrease were accounted for by inspiratory rib cage (RCM,i) and abdominal (ABM) muscle action, respectively. The pressure developed by RCM,i and ABM and Pdi progressively increased (P < 0.05) from rest to the highest workload. The increase in V(di), more than the increase in the change in Pdi, accounted for the increase in Wdi. In conclusion, we found that, in walking healthy humans, the increase in ventilatory demand was met by the recruitment of the inspiratory and expiratory reserve volume. ABM action accounted for the expiratory reserve volume recruitment. We have also shown that the diaphragm acts mainly as a flow generator. The rib cage distortion, although measurable, is minimized by the coordinated action of respiratory muscles.     

Reflex effect of esophageal distension on respiratory muscle activity and pressure

The electrical activity of the respiratory skeletal muscles is altered in response to reflexes originating in the gastrointestinal tract. The present study evaluated the reflex effects of esophageal distension (ED) on the distribution of motor activity to both inspiratory and expiratory muscles of the rib cage and abdomen and the resultant changes in thoracic and abdominal pressure during breathing. Studies were performed in 21 anesthetized spontaneously breathing dogs. ED was produced by inflating a balloon in the distal esophagus. ED decreased the activity of the costal and crural diaphragm and external intercostals and abolished all preexisting electrical activity in the expiratory muscles of the abdominal wall. On the other hand, ED increased the activity of the parasternal intercostals and expiratory muscles located in the rib cage (i.e., triangularis sterni and internal intercostal). All effects of ED were graded, with increasing distension exerting greater effects, and were eliminated by vagotomy. The effect of increases in chemical drive and lung inflation reflex activity on the response to ED was examined by performing ED while animals breathed either 6.5% CO2 or against graded levels of positive end-expiratory pressure (PEEP), respectively. Changes in respiratory muscle electrical activity induced by ED were similar (during 6.5% CO2 and PEEP) to those observed under control conditions. We conclude that activation of mechanoreceptors in the esophagus reflexly alters the distribution of motor activity to the respiratory muscles, inhibiting the muscles surrounding the abdominal cavity and augmenting the parasternals and expiratory muscles of the chest wall.     

Analysis of human chest wall motion using a two-compartment rib cage model.

We present a model of chest wall mechanics that extends the model described previously by Macklem et al. (J. Appl. Physiol. 55: 547-557, 1983) and incorporates a two-compartment rib cage. We divide the rib cage into that apposed to the lung (RCpul) and that apposed to the diaphragm (RCab). We apply this model to determine rib cage distortability, the mechanical coupling between RCpul and RCab, the contribution of the rib cage muscles to the pressure change during spontaneous inspiration (Prcm), and the insertional component of transdiaphragmatic pressure in humans. We define distortability as the relationship between distortion and transdiaphragmatic pressure (Pdi) and mechanical coupling as the relationship between rib cage distortion and the pressure acting to restore the rib cage to its relaxed configuration (Plink), as assessed during bilateral transcutaneous phrenic nerve stimulation. Prcm was calculated at end inspiration as the component of the pressure displacing RCpul not accounted for by Plink or pleural pressure. Prcm and Plink were approximately equal during quiet breathing, contributing 3.7 and 3.3 cmH2O on average during breaths associated with a change in Pdi of 3.9 cmH2O. The insertional component of Pdi was measured as the pressure acting on RCab not accounted for by the change in abdominal pressure during an inspiration without rib cage distortion and was 40 +/- 12% (SD) of total Pdi. We conclude that there is substantial resistance of the human rib cage to distortion, that, along with rib cage muscles, contributes importantly to the fall in pleural pressure over the costal surface of the lung.     

Voluntary changes of thoracoabdominal shape and regional lung volumes in humans.

We measured regional lung volumes from apex to base in humans during changes in thoracoabdominal shape which we monitored with magnetometers. In erect subjects, voluntary changes of shape at FRC did not change regional volume distribution. In supine subjects, the effect of negative pressure applied to the abdomen and a similar thoracoabdominal configuration achieved by voluntary means were studied. The distribution of regional volumes in both situations was the same as that measured during relaxation at the same overall lung volumes. We concluded that neither voluntary changes in shape nor negative abdominal pressure influenced the human pleural pressure gradient. This result, which differed from findings in animals, was probably because the human chest was relatively stiff and behaved with one degree of freedom; all parts of the human rib cage changed dimensions proportionally while negative abdominal pressure distorted the rib cage of animals.     

Relationships between abdominal and diaphragmatic volume displacements

We investigated the relationship between the volumes displaced by the diaphragm and the abdominal wall during spontaneous breathing in supine anesthetized dogs. Diaphragmatic volume displacement (Vdi) was calculated from measurements taken from anteroposterior fluoroscopic images employing a previously described geometric model. The volume displacement of the abdominal wall (Vabd) was measured with a calibrated Respitrace. Shortening of single diaphragm muscle bundles in costal and crural regions was measured as the distance between radiopaque beads sutured to the peritoneal surface of the muscle. We found that Vdi always exceeded Vabd, but Vabd/Vdi was larger in animals in which the abdominal wall was more compliant. In this preparation, Vdi is better correlated with costal than with crural shortening. Vabd did not correlate with either costal or crural shortening. We infer that the difference between Vdi and Vabd reflects the volume displacement of the lower rib cage caused by diaphragm contraction. This volume difference was tightly correlated with costal shortening. We conclude from these data that coupling between Vdi and Vabd is influenced by the relative compliances of the chest wall and abdomen. Shortening of regions of the diaphragm may have variable relationships to the measured volume displacement, but costal shortening is intimately related to expansion of the lower rib cage.     

Chest wall motion and expiratory muscle use during phonation in normal humans

The pattern of rib cage (RC) and abdomen (AB) motion and the electromyograms of the triangularis sterni (TS) and abdominal external oblique (EO) muscles were studied during speech and reading in six normal uninformed subjects in the sitting posture. Most phrases were started from within the tidal breathing range and extended below RC and AB spontaneous end-expiratory volumes. On the average, 75% of the change in chest wall volume occurred below the resting end-expiratory level. The expired volume resulted from a large predominance of RC displacement, and this was accompanied by marked recruitment of the TS. The EO was also generally activated, but the pattern of activation was less consistent. We conclude that 1) speech occurs primarily below the spontaneous end-expiratory level; 2) most of the volume change is caused by active emptying of the RC produced, at least in part, by contraction of the TS; 3) concomitant activation of the abdominal muscles serves to optimize the inspiratory function of the diaphragm, which has to contract rapidly between phrases to refill the respiratory system.     

Chest wall motion during epidural anesthesia in dogs

To determine the relative contribution of rib cage and abdominal muscles to expiratory muscle activity during quiet breathing, we used lumbar epidural anesthesia in six pentobarbital sodium-anesthetized dogs lying supine to paralyze the abdominal muscles while leaving rib cage muscle motor function substantially intact. A high-speed X-ray scanner (Dynamic Spatial Reconstructor) provided three-dimensional images of the thorax. The contribution of expiratory muscle activity to tidal breathing was assessed by a comparison of chest wall configuration during relaxed apnea with that at end expiration. We found that expiratory muscle activity was responsible for approximately half of the changes in thoracic volume during inspiration. Paralysis of the abdominal muscles had little effect on the pattern of breathing, including the contribution of expiratory muscle activity to tidal breathing, in most dogs. We conclude that, although there is consistent phasic expiratory electrical activity in both the rib cage and the abdominal muscles of pentobarbital-anesthetized dogs lying supine, the muscles of the rib cage are mechanically the most important expiratory muscles during quiet breathing.     

Role of rib cage elastance in the coupling between the abdominal muscles and the lung.

The abdominal muscles expand the rib cage when they contract alone. This expansion opposes the deflation of the lung and may be viewed as pressure dissipation. The hypothesis was raised, therefore, that alterations in rib cage elastance should affect the lung deflating action of these muscles. To test this hypothesis and evaluate the quantitative importance of this effect, we measured the changes in airway opening pressure (Pao), abdominal pressure (Pab), and rib cage transverse diameter during isolated stimulation of the transversus abdominis muscle in anesthetized dogs, first with the rib cage intact and then after rib cage elastance was increased by clamping the ribs and the sternum. Stimulation produced increases in Pao, Pab, and rib cage diameter in both conditions. With the ribs and sternum clamped, however, the change in Pab was unchanged but the change in Pao was increased by 77% (P < 0.001). In a second experiment, the transversus abdominis was stimulated before and after rib cage elastance was reduced by removing the bony ribs 3-8. Although the change in Pab after removal of the the ribs was still unchanged, the change in Pao was reduced by 62% (P < 0.001). These observations, supported by a model analysis, indicate that rib cage elastance is a major determinant of the mechanical coupling between the abdominal muscles and the lung. In fact, in the dog, the effects of rib cage elastance and Pab on the lung-deflating action of the abdominal muscles are of the same order of magnitude.     

Vagal contributions to respiratory muscle activity during eupnea in the awake dog.

We examined the effects of reversible vagal cooling on respiratory muscle activities in awake chronically instrumented tracheotomized dogs. We specifically analyzed electromyographic (EMG) activity and its ventilatory correlates, end-expiratory lung volume (EELV) and diaphragmatic resting length via sonomicrometry. Elimination of phasic and tonic mechanoreceptor activity by vagal cooling doubled the EMG activity of the costal, crural, and parasternal muscles, with activation occurring sooner relative to the onset of inspiratory flow. Diaphragmatic postinspiration inspiratory activity in the intact dog coincided with a brief mechanical shortening of the diaphragm during early expiration; vagal blockade removed both the electrical activity and the mechanical shortening. Vagal blockade also doubled the EMG activity of a rib cage expiratory muscle, the triangularis sterni, but reduced that of an abdominal expiratory muscle, the transversus abdominis. Within-breath electrical activity of both muscles occurred sooner relative to the onset of expiratory flow during vagal blockade. Vagal cooling was also associated with a 12% increase in EELV and a 5% decrease in end-expiratory resting length of the diaphragm. We conclude that vagal input significantly modulates inspiratory and expiratory muscle activities, which help regulate EELV efficiently and optimize diaphragmatic length during eupneic breathing in the awake dog.     

Chest wall kinematic determinants of diaphragm length by optoelectronic plethysmography and ultrasonography.

To estimate diaphragm fiber length from thoracoabdominal configuration, we measured axial motion of the right-sided area of apposition by ultrasonography and volumes displaced by chest wall compartments [pulmonary, abdominal rib cage, and abdomen (Vab)] by optoelectronic plethysmography in four normal men during quiet breathing and incremental exercise without and with expiratory flow limitation. Points at the cephalic area of apposition border were digitized from echo images and mapped into three-dimensional space, and the axial distance from the xyphoidal transverse plane (D(ap)) was measured simultaneously with the volumes. Linear regression analysis between changes (Delta) in D(ap) and the measured volume changes under all conditions showed that 1) DeltaD(ap) was linearly related more to DeltaVab than to changes in pulmonary and abdominal rib cage volumes; and 2) this was highly repeatable between measures. Multiple stepwise regression analysis showed that DeltaVab accounted for 89-96% of the variability of DeltaD(ap), whereas the rib cage compartments added <1%. We conclude that, under conditions of quiet breathing and exercise, with and without expiratory flow limitation, instantaneous DeltaD(ap) can be estimated from DeltaVab.     

Volume infusion produces abdominal distension, lung compression, and chest wall stiffening in pigs.

The effect of severe generalized edema on respiratory system mechanics is not well described. We measured airway pressure, gastric pressure, and four vertical pleural pressures in 13 anesthetized paralyzed pigs ventilated in the upright position. Pressure-volume relationships of the respiratory system, chest wall, and lung were measured on deflation from total lung capacity to residual volume and during tidal breathing both before (control) and 50 min after one of two interventions. In one series of experiments, a volume equal to 15-20% of the pig's body weight was infused intravenously. In a second series, a balloon was placed in the peritoneal space to distend the abdomen to the same gastric pressures as achieved in the first series. Measurements were compared before and after either abdominal balloon inflation or volume infusion. Volume infusion increased the pleural pressure in dependent lung regions, decreased both total lung capacity (34%) and functional residual capacity (62%) (both P less than 0.05), and markedly shifted the respiratory system and chest wall pressure-volume curves to the right, but it only moderately affected the lung deflation curve. Tidal compliances of the respiratory system, chest wall, and lung decreased 36, 31, and 49%, respectively (all P less than 0.05). The effect of abdominal balloon inflation on respiratory system mechanics was similar to that of volume infusion. We conclude that infusing large volumes of fluid markedly alters chest wall mechanics, mainly by causing abdominal distension that prohibits descent of the diaphragm.     

Effect of mechanical loading on displacements of chest wall during breathing in humans

Using a respiratory inductive plethysmograph (Respitrace) we studied thoracoabdominal movements in eight normal subjects during inspiratory resistive (Res) and elastic (El) loading. The magnitude of loads was chosen so as to produce a fall in inspiratory mouth pressure of 20 cmH2O. The contribution of rib cage (RC) to tidal volume (VT) increased significantly from 68% during quiet breathing (QB) to 74% during El and 78% during Res. VT and breathing frequency did not change significantly. During loading a phase lag was present on inspiration so that the abdomen led the rib cage. However, outward movement of the abdomen ceased in the latter part of inspiration, and the RC became the sole contributor to VT. These observations suggest greater recruitment of the inspiratory musculature of the RC than the diaphragm during loading, although changes in the mechanical properties of the chest wall may also have contributed. Indeed, an increase in abdominal end-expiratory and end-inspiratory pressures was observed in five out of six subjects, indicating abdominal muscle recruitment which may account for part of the reduction in abdominal excursion. Both Res and El increased the rate of emptying of the respiratory system during the ensuing unloaded expiration as a result of a reduction in rib cage expiratory-braking mechanisms. The time course of abdominal displacements during expiration was unaffected by loading.     

Mechanics of compartmental models of the chest wall

Standard methods for describing the mechanical properties of a linear elastic system are applied to the two- and three-compartment models of the chest wall. The compliance matrix and the experiments required to determine the entries in this matrix and thereby to describe the mechanical properties of the relaxed chest wall are described. The effective forces exerted by external loads and muscle tension are defined. The formal theory is used to identify relations among variables. From the definition of effective force, it follows that the ratio of the forces exerted by the diaphragm on the rib cage and abdomen is the same as the ratio of the dependence of diaphragm length on rib cage and abdominal volumes. As an example of relations among variables that follow from the symmetry of the compliance matrix, it is shown that the change of gastric pressure caused by raising pleural pressure is related to the change in lung volume caused by changing stomach volume.     

Effect of intravenous midazolam on breathing pattern and chest wall mechanics in human

Breathing pattern, thoracoabdominal motion, and separate end-expiratory positions of the rib cage and abdomen were measured noninvasively in eight healthy subjects before and after intravenous administration of either placebo or midazolam, a short-acting benzodiazepine. Compared with placebo, midazolam produced a significant (P less than 0.01) decrease in mean inspiratory flow of 29% from preinjection values, resulting in a 39% reduction in tidal volume (VT). This ventilatory depression was partly compensated by a 35% decrease in expiratory time producing an increase in respiratory rate (+39%). The fall in VT was almost entirely (91%) mediated by a reduction of the abdominal contribution to tidal breathing while sparing rib cage motion. This fact contrasts with the effects of inhalational anesthetics or morphine, which preferentially depress rib cage expansion, indicating that thoracoabdominal motion may selectively be depressed by different pharmacological agents. In addition, continuous recording of end-expiratory levels showed a significant transient fall in the rib cage's end-tidal position 2 min after midazolam administration associated with the occurrence of central apneas.