A model approach to assess diaphragmatic volume displacement

Diaphragmatic volume displacement (Vdi) is calculated from two models using measurements obtained from anteroposterior fluoroscopic images of supine anesthetized dogs. In model 1, diaphragmatic descent was treated as if it were a "piston in a cylinder." In contrast, model 2 incorporated thoracic configuration as well as inspiratory changes in rib cage diameter and diaphragm shape. In one dog, a computerized tomography reconstruction of Vdi was compared with Vdi calculated using the models. Vdi calculated from model 2 lay within 11% of the computerized tomographic value, whereas Vdi based on model 1 was 30% larger. In seven animals, radiopaque markers were sewn to the right costal diaphragm. Digitized fluoroscopic images were used to measure intermarker distance, an index of muscle shortening. For four tidal breaths per dog, in model 2 Vdi averaged 49 +/- 18% of tidal volume and was weakly correlated with costal diaphragm muscle shortening (R = 0.74). It is concluded that Vdi can be estimated from linear dimensions in the coronal plane, provided that inspiratory changes in rib cage diameter and diaphragmatic shape change are taken into account.     

Mechanical coupling of upper and lower canine rib cages and its functional significance

We studied rib cage distortability and reexamined the mechanical action of the diaphragm and the rib cage muscles in six supine anesthetized dogs by measuring changes in upper rib cage cross-sectional area (Aurc) and changes in lower rib cage cross-sectional area (Alrc) and the respective pressures acting on them. During quiet breathing in the intact animal the rib cage behaved as a unit (Aurc: 14.6 +/- 7.9 vs. Alrc: 15.1 +/- 9.6%), whereas considerable distortions of the rib cage occurred during breathing after bilateral phrenicotomy (Aurc: 21.0 +/- 5.1 vs. Alrc: 7.0 +/- 4.8%). These distortions were even more pronounced during phrenic nerve stimulation and separate stimulation of the costal and crural parts of the diaphragm (e.g., phrenic nerve stimulation; Aurc: -7.1 +/- 5.1 vs. Alrc: 6.9 +/- 3.5%). During the latter maneuvers the upper rib cage deflated along the relationship between upper rib cage dimensions and pleural pressure obtained during passive deflation, whereas the lower rib cage inflated close to the relationship between lower rib cage dimensions and abdominal pressure obtained during passive inflation. The latter relationship is expected to differ between costal and crural stimulation, since costal action has both an appositional and insertional component and crural action only has an appositional component. The difference between costal and crural stimulation, however, was relatively small, and the slopes were only slightly steeper for the costal than for the crural stimulation (2.9 +/- 1.2 vs. 2.2 +/- 1.0%.(ABSTRACT TRUNCATED AT 250 WORDS)     

Volume quantification of chest wall motion in dogs

We employed high-speed multisliced X-ray-computed tomography to determine the relative volume contributions of rib cage (delta Vrc) and diaphragmatic motion (delta Vdi) to tidal volume (VT) during spontaneous breathing in 6 anesthetized dogs lying supine. Mean values were 40 +/- 6% (SE) for delta Vrc and 62 +/- 8% of VT for delta Vdi. The difference between VT and changes in thoracic cavity volume was taken to represent a change in thoracic blood volume (2 +/- 3% of VT). To estimate how much of delta Vrc was caused by diaphragmatic contraction and how much of delta Vdi was caused by rib cage motion, delta Vrc and delta Vdi were determined during bilateral stimulation of the C5-C6 phrenic nerve roots in the apneic dog and again during spontaneous breathing after phrenicotomy. Thoracic cavity volume (Vth) measured during hypocapnic apnea was consistently larger than Vth at end expiration, suggesting that relaxation of expiratory muscles contributed significantly to both delta Vrc and delta Vdi during spontaneous inspiration. Phrenic nerve stimulation did not contribute to delta Vrc, suggesting that diaphragmatic contraction had no net expanding action on the rib cage above the zone of apposition. Spontaneous breathing after phrenicotomy resulted in small and inconsistent diaphragmatic displacement (8 +/- 4% of VT). We conclude that the diaphragm does not drive the rib cage to inflate the lungs and that rib cage motion does not significantly affect diaphragmatic position during spontaneous breathing in anesthetized dogs lying supine.     

Regional deformation of the canine diaphragm.

To follow regional deformation of the diaphragm in dogs, radiopaque markers were implanted under surgical anesthesia into different anatomic regions of the muscle in triangular arrays (approximately 1 cm to a side). After recovery from surgery, changes in area and shape of the triangles were followed with biplane cinefluorography during quiet breathing and during inspiratory efforts against an occluded airway (Mueller maneuvers). From changes in shape of the triangles during contraction, area changes were decomposed into a major direction and magnitude of shortening (Eg1) and a minor length change (Eg2) perpendicular to Eg1, both expressed as a fraction of initial length at end expiration. With the use of these techniques, systematic differences in regional area change were observed in different parts of the diaphragm during inspiratory efforts at different lung volumes. Regional area always decreased during contraction in the crural and midcostal zones of apposition to the rib cage. Area decreased less and often increased during inspiratory efforts in the costal dome near the central tendon and in the costal region near its rib cage insertion. Differences in regional area change were not due to differences in the Eg1 in different parts of the diaphragm but were a consequence of differences in widening of the muscle along Eg2 perpendicular to the direction of Eg1. As lung volume was passively increased above functional residual capacity, regional area decreased in all parts of the diaphragm except in the costal regions near rib cage insertion, where area increased.     

Ratio of active to passive muscle shortening in the canine diaphragm.

Active and passive shortening of muscle bundles in the canine diaphragm were measured with the objective of testing a consequence of the minimal-work hypothesis: namely, that the ratio of active to passive shortening is the same for all active muscles. Lengths of six muscle bundles in the costal diaphragm and two muscle bundles in the crural diaphragm of each of four bred-for-research beagle dogs were measured by the radiopaque marker technique during the following maneuvers: a passive deflation maneuver from total lung capacity to functional residual capacity, quiet breathing, and forceful inspiratory efforts against an occluded airway at different lung volumes. Shortening per liter increase in lung volume was, on average, 70% greater during quiet breathing than during passive inflation in the prone posture and 40% greater in the supine posture. For the prone posture, the ratio of active to passive shortening was larger in the ventral and midcostal diaphragm than at the dorsal end of the costal diaphragm. For both postures, active shortening during quiet breathing was poorly correlated with passive shortening. However, shortening during forceful inspiratory efforts was highly correlated with passive shortening. The average ratios of active to passive shortening were 1.23 +/- 0.02 and 1.32 +/- 0.03 for the prone and supine postures, respectively. These data, taken together with the data reported in the companion paper (T. A. Wilson, M. Angelillo, A. Legrand, and A. De Troyer, J. Appl. Physiol. 87: 554-560, 1999), support the hypothesis that, during forceful inspiratory efforts, the inspiratory muscles drive the chest wall along the minimal-work trajectory.     

Velocity of shortening of inspiratory muscles and inspiratory flow

Respiratory muscle length was measured with sonomicrometry to determine the relation between inspiratory flow and velocity of shortening of the external intercostal and diaphragm. Electromyographic (EMG) activity and tidal shortening of the costal and crural segments of the diaphragm and of the external intercostal were recorded during hyperoxic CO2 rebreathing in 12 anesthetized dogs. We observed a linear increase of EMG activity and peak tidal shortening of costal and crural diaphragm with alveolar CO2 partial pressure. For the external intercostal, no consistent pattern was found either in EMG activity or in tidal shortening. Mean inspiratory flow was linearly related to mean velocity of shortening of costal and crural diaphragm, with no difference between the two segments. Considerable shortening occurred in costal and crural diaphragm during inspiratory efforts against occlusion. We conclude that the relation between mean inspiratory flow and mean velocity of shortening of costal and crural diaphragm is linear and can be altered by an inspiratory load. There does not appear to be a relationship between inspiratory flow and velocity of shortening of external intercostals.     

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.     

A model of inspiratory muscle mechanics

We have previously shown that the costal and crural parts of the diaphragm have different actions on the rib cage (RC) and that the tension developed in one part is not transmitted perfectly to the other. Thus the diaphragm can be modeled pneumatically or electrically as two generators or pumps in series between the lung and abdomen. As such, the force developed by diaphragmatic contraction is the sum of the forces developed in each part, whereas the volume displaced is the same for each part and equal to the total volume displaced. The costal part of the diaphragm is in series with the intercostal and accessory (IA) muscles between the lung and RC, whereas the crural part is in parallel. The volume displaced by simultaneous contraction of the crural part and IA is the sum of volumes displaced by each part. The action of pleural and abdominal pressure [acting through the area of apposition (Aap) of the diaphragm to RC] can be modelled as a summing junction between IA and RC. With hyperinflation the costal part acts more and more in parallel with both IA and the crural part, whereas Aap diminishes, so that the ability to develop large forces decreases independently of the muscles' force-length relationships. The model also predicts that the factors determining the length of the costal and crural parts are different. Finally, the parallel and serial arrangement of the inspiratory musculature allows for increases in maximum power, maximum force, and maximum velocity by appropriate recruitment of the various muscle groups.     

Effect of intestinal afferent stimulation on pattern of respiratory muscle activation

The purpose of the present study was to examine the reflex effects of mechanical stimulation of intestinal visceral afferents on the pattern of respiratory muscle activation. In 14 dogs anesthetized with pentobarbital sodium, electromyographic activity of the costal and crural diaphragm, parasternal intercostal, and upper airway respiratory muscles was measured during distension of the small intestine. Rib cage and abdominal motion and tidal volume were also recorded. Distension produced an immediate apnea (11.16 +/- 0.80 s). During the first postapneic breath, costal (43 +/- 7% control) and crural (64 +/- 6% control) activity were reduced (P less than 0.001). In contrast, intercostal (137 +/- 11%) and upper airway muscle activity, including alae nasi (157 +/- 16%), genioglossus (170 +/- 15%), and posterior cricoarytenoid muscles (142 +/- 7%) all increased (P less than 0.005). There was greater outward rib cage motion although the abdomen moved paradoxically inward during inspiration, resulting in a reduction in tidal volume (82 +/- 6% control) (P less than 0.005). Postvagotomy distension produced a similar apnea and subsequent reduction in costal and crural activity. However, enhancement of intercostal and upper airway muscle activation was abolished and there was a greater fall in tidal volume (65 +/- 14%). In conclusion, mechanical stimulation of intestinal afferents affects the various inspiratory muscles differently; nonvagal afferents produce an initial apnea and subsequent depression of diaphragm activity whereas vagal pathways mediate selective enhancement of intercostal and upper airway muscle activation.     

Determinants of transdiaphragmatic pressure in dogs

We measured the transdiaphragmatic pressure (Pdi) during bilateral phrenic nerve stimulation and evaluated the determinants of its change with lung volume, chest wall geometry, and respiratory system impedance in supine dogs. Four rows of radiopaque markers were sewn onto muscle bundles of the costal and crural diaphragm between their origin on the central tendon and their insertion on the rib cage and spine. The length of the diaphragm (L) was determined from the projection images of marker rows using biplane fluoroscopy. Measurements were made at lung volumes between total lung capacity and functional residual capacity before and after the infusion of Ringer lactate solution into the abdominal cavity. In contrast to relaxation, during tetanic stimulation the active lengths of the muscle bundles were similar at all volumes, but the diaphragm assumed different shapes. Although the small differences in active muscle length with volume and liquid loads are consistent with only small changes in muscle force output, Pdi varied by a factor of greater than or equal to 5. There was no single L/Pdi curve that fitted all data during 50-Hz stimulations. We conclude that under these experimental conditions Pdi is not a unique measure of the force produced by the diaphragm and that lung volume, chest wall geometry, and respiratory system impedance are important determinants of the mechanical efficiency of the diaphragm as a pressure generator.     

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.     

In vivo regional diaphragm function in dogs

A biplane videofluorographic system was used to track the position of metallic markers affixed to the abdominal surface of the left hemidiaphragm in supine anesthetized dogs. Regional shortening was determined from intermarker distances of rows of markers placed along muscle bundles in the ventral, middle, and dorsal regions of the costal diaphragm and of one row on the crural diaphragm. Considerable variability of regional shortening was seen in a given row, which was reproducible on repeat study in individual dogs but which differed between mechanical ventilation and spontaneous breathing. There were no consistent patterns among dogs. Regional shortening obtained from the change in length of rows extending from chest wall to central tendon showed no consistent differences among dogs during spontaneous breathing. At equal tidal volumes, all regions (except the ventral costal diaphragm) shortened more during spontaneous breathing than during mechanical ventilation.     

Relationship between diaphragm length and abdominal dimensions

We examined the relationship between changes in abdominal cross-sectional area, measured by respiratory inductive plethysmography, and changes in length in the costal and crural parts of the diaphragm, measured by sonomicrometry, in nine supine, anesthetized dogs. During passive inflation, both parts of the diaphragm shortened and abdominal cross-sectional area increased. During passive deflation, both parts of the diaphragm lengthened and abdominal cross-sectional area decreased. We subsequently used the relationship between costal and crural diaphragmatic length, respectively, and abdominal cross-sectional area during passive inflation-deflation to predict the length changes in the costal and crural diaphragm during quiet breathing before and after bilateral phrenicotomy. In the intact animal the inspiratory shortening in the crural diaphragm was almost invariably greater than predicted from the relationship during passive inflation. During inspiration after phrenicotomy the crural diaphragm invariably lengthened, whereas the costal diaphragm often shortened. In general there was a good correlation between the measured and predicted length change for the crural diaphragm (r = 0.72 before and 0.79 after phrenicotomy) and a poor one for the costal diaphragm (r = 0.05 before and 0.19 after phrenicotomy).     

Relationship between axial motion and volume displacement of the diaphragm during VC maneuvers.

During semistatic inspiratory and expiratory vital capacity (VC) maneuvers, axial motion of the diaphragm was measured by lateral fluoroscopy and was compared with diaphragmatic volume displacement. Axial motion was measured at the anterior, middle, and posterior parts of the diaphragm, and the mean of these measurements was used. The volume displacement was calculated in two ways: first, from respiratory inductive plethysmograph-(Respitrace) derived cross-sectional area changes of rib cage and abdomen (Vdi,RIP) by means of a theoretical analysis described by Mead and Loring (J. Appl. Physiol. 53: 750-755, 1982) and, second, from fluoroscopically measured changes in position and anteroposterior surface of the diaphragm (Vdi,F). A very good linear relationship was found between Vdi,RIP and Vdi,F during inspiration as well as expiration (r greater than 0.95), indicating that the analysis of Mead and Loring was valid in the conditions of the present study. The diaphragmatic volume displacement (active or passive) accounted for 50-60% of VC. A very good linear relationship was also found between mean axial motion and volume displacement of the diaphragm measured with both methods during inspiration and expiration (r greater than 0.98). Our data suggest that, over the VC range, diaphragmatic displacement functionally can be represented by a pistonlike model, although topographically and anatomically it does not behave as a piston.     

Effect of hyperinflation and equalization of abdominal pressure on diaphragmatic action

We tested the hypothesis that the mechanical arrangement of costal (COS) and crural (CRU) diaphragms can be changed from parallel to series when direct or indirect transmission of tension occurs. Ratio of rib cage to abdominal displacement (RC/AB) resulting from separate COS and CRU stimulations were used to measure RC expanding action. Hyperinflation in six dogs caused RC/AB with COS and CRU stimulations to change progressively from 0.53 +/- 0.07 (SE) and 0.03 +/- 0.05 at functional residual capacity (FRC) to -0.48 +/- 0.08 and -0.46 +/- 0.05 at 68% inspiratory capacity, respectively. Liquid substitution of abdominal contents in six other dogs equalized abdominal pressure swings (delta Pab), without changing chest wall elastic properties or geometry, or costal RC/AB (0.35 +/- 0.07 before and 0.33 +/- 0.06 after) but caused crural RC/AB to change from 0.01 +/- 0.05 to 0.31 +/- 0.01. We conclude that hyperinflation changes fiber orientation, allowing direct transmission of tension between COS and CRU, which become linked mechanically in series (the diaphragm acts as a unit with RC deflating action); and equalization of delta Pab causes indirect transmission of tension between COS and CRU, which become linked in series (the diaphragm acts as a unit with RC inflating action).     

Videofluoroscopic assessment of muscle fiber shortening in the in situ canine diaphragm

We tested the hypothesis that dynamic shortening of the costal diaphragm can be accurately estimated from measurements of the radiographic width of the zone of apposition (WZapp) by studying seven supine anesthetized dogs. Both muscle fiber length, represented by the distance between implanted radiopaque markers, and WZapp were measured from digitized recordings of fluoroscopic images utilizing interactive computer software. The WZapp was highly correlated with the length of costal fibers during active respiration in all animals (mean R2 = 0.94). The accuracy in the prediction of fiber length and shortening during breathing is enhanced by inclusion of additional variables describing the displacement of the abdominal wall and the resting geometric orientation of the fibers. We conclude that dynamic fluoroscopic measurement of WZapp is a valuable technique for estimating dynamic diaphragm fiber length and shortening. Depending on the experimental circumstances, WZapp may be a more easily acquired indicator of diaphragm shortening than other variables that have been previously utilized. As such, it may provide a suitable approach to assess active shortening of the diaphragm in humans.     

Chest wall motion during spontaneous breathing and mechanical ventilation in dogs

We measured the volume change of the thoracic cavity (delta Vth) and the volumes displaced by the diaphragm (delta Vdi) and rib cage (delta Vrc) in six pentobarbital-anesthetized dogs lying supine. A high-speed X-ray scanner (dynamic spatial reconstructor) provided three-dimensional images of the thorax during spontaneous breathing and during mechanical ventilation with paralysis. Tidal volume (VT) was measured by integrating gas flow. Changes in thoracic liquid volume (delta Vliq, presumably caused by changes in thoracic blood volume) were calculated as delta Vth - VT. Absolute volume displaced by the rib cage was not significantly different during the two modes of ventilation. During spontaneous breathing, thoracic blood volume increased during inspiration; delta Vliq was 12.3 +/- 4.1% of delta Vth. During mechanical ventilation, delta Vliq was nearly zero. Configuration of the relaxed chest wall was similar during muscular relaxation induced by either pharmacological paralysis or hyperventilation. Expiratory muscle activity produced 50 +/- 11% of the delta Vth during spontaneous breathing. We conclude that at constant VT the volume displaced by the rib cage is remarkably similar during the transition from spontaneous breathing to mechanical ventilation, while both diaphragmatic volume displacement and changes in intrathoracic blood volume decrease by a similar amount.     

Respiratory muscle length measured by sonomicrometry

The use of sonomicrometry to study the mechanical properties of the diaphragm in vivo is presented. This method consists of the implantation of piezoelectric transducers between muscle fibers to measure the fibers' changes in length. Ultrasonic bursts are produced by one transducer upon electrical excitation and sensed by a second transducer placed 1-2 cm away. The time elapsed between the generation of the ultrasound burst and its detection is used to calculate the intertransducer distance. Excitation and sampling are done at 1.5 kHz and the output is a DC signal proportional to the length change between the transducers. Neither irreversible injury to the diaphragm nor regional differences within an anatomical part or segment were noted. Measurements were stable within the physiological range of temperature. We measured costal and crural length and velocity of contraction in anesthetized dogs during spontaneous breathing, occluded inspirations, passive lung inflation, and supramaximal phrenic nerve stimulation. We found that shortening during spontaneous breathing was 11 and 6% for crural and costal, respectively. The crural leads the costal in velocity of shortening. Supramaximal stimulation results in a velocity of shortening of 5 resting lengths X s-1. During an occluded inspiration crural shortens as much as in the nonoccluded breath, whereas costal shortens less. During passive lung inflation there is a nearly linear relationship between lung volume and diaphragm length; however, the relationships of chest wall dimensions with diaphragm length are nonlinear and cannot be described by any simple function. Some of the implications of these data on the present understanding of diaphragmatic mechanics are discussed.     

Crural diaphragm inhibition during esophageal distension correlates with contraction of the esophageal longitudinal muscle in cats

Esophageal distension causes simultaneous relaxation of the lower esophageal sphincter (LES) and crural diaphragm. The mechanism of crural diaphragm relaxation during esophageal distension is not well understood. We studied the motion of crural and costal diaphragm along with the motion of the distal esophagus during esophageal distension-induced relaxation of the LES and crural diaphragm. Wire electrodes were surgically implanted into the crural and costal diaphragm in five cats. In two additional cats, radiopaque markers were also sutured into the outer wall of the distal esophagus to monitor esophageal shortening. Under light anesthesia, animals were placed on an X-ray fluoroscope to monitor the motion of the diaphragm and the distal esophagus by tracking the radiopaque markers. Crural and costal diaphragm electromyograms (EMGs) were recorded along with the esophageal, LES, and gastric pressures. A 2-cm balloon placed 5 cm above the LES was used for esophageal distension. Effects of baclofen, a GABA(B) agonist, were also studied. Esophageal distension induced LES relaxation and selective inhibition of the crural diaphragm EMG. The crural diaphragm moved in a craniocaudal direction with expiration and inspiration, respectively. Esophageal distension-induced inhibition of the crural EMG was associated with sustained cranial motion of the crural diaphragm and esophagus. Baclofen blocked distension-induced LES relaxation and crural diaphragm EMG inhibition along with the cranial motion of the crural diaphragm and the distal esophagus. There is a close temporal correlation between esophageal distension-mediated LES relaxation and crural diaphragm inhibition with the sustained cranial motion of the crural diaphragm. Stretch caused by the longitudinal muscle contraction of the esophagus during distension of the esophagus may be important in causing LES relaxation and crural diaphragm inhibition.     

Regional differences in myosin heavy chain isoforms and enzyme activities of the rat diaphragm.

Myosin heavy chain isoforms and enzyme activities were compared between the costal and crural regions of the rat diaphragm. The percentage of heavy chain (HC) IIb in the crural region of the diaphragm was significantly (P less than 0.05) higher than that in the costal region (mean 7.3 vs. 3.0%), and the percentage of HCI was significantly lower in the crural than in the costal diaphragm (22.7 vs. 27.9%). The distributions of HCIIa and HCIId were relatively homogeneous in both regions. Succinate dehydrogenase activity in the costal diaphragm was 21% greater (P less than 0.01) than in the crural diaphragm. In contrast, there was no significant difference in the activity of phosphofructokinase in the crural and costal diaphragms. These results demonstrate that a difference in myosin heavy chain isoforms and oxidative capacity exists between the costal and crural regions of the rat diaphragm.